ENDANGERED SPECIES RESEARCHEndang Species Res

Vol 45 251ndash268 2021httpsdoiorg103354esr01137

Published July 29sect

1 INTRODUCTION

The management and conservation of migratoryspecies is challenging particularly in dynamic mar-ine environments Many factors influence a speciesrsquopresence so it is difficult to predict how and when a

species may utilize an area and whether conserva-tion actions are necessary Anthropogenic stressorscan also affect a speciesrsquo presence or residency andimpact the quality of suitable habitats throughout themigratory route needed for the speciesrsquo breedingfood and shelter (Runge et al 2014) Thus the effec-

copy The authors 2021 Open Access under Creative Commons byAttribution Licence Use distribution and reproduction are un -restricted Authors and original publication must be credited

Publisher Inter-Research middot wwwint-rescom

Corresponding author tetequintanacomcastnet

Residency demographics and movement patternsof North Atlantic right whales Eubalaena glacialisin an offshore wind energy development area in

southern New England USA

E Quintana-Rizzo15 S Leiter1 T V N Cole2 M N Hagbloom1 A R Knowlton1 P Nagelkirk1 O OrsquoBrien1 C B Khan2 A G Henry2 P A Duley2 L M Crowe3

C A Mayo4 S D Kraus1

1Anderson Cabot Center for Ocean Life New England Aquarium Boston MA 02110 USA2Northeast Fisheries Science Center National Marine Fisheries Service National Oceanic and Atmospheric Administration

Woods Hole MA 02543 USA3Integrated Statistics under contract to the Northeast Fisheries Science Center National Marine Fisheries Service

National Oceanic and Atmospheric Administration Woods Hole MA 02543 USA4Center for Coastal Studies Provincetown MA 02657 USA

5Present address Simmons University Boston MA 02115 USA

ABSTRACT Offshore wind energy development is growing quickly around the world In south-ern New England USA one of the largest commercial offshore wind energy farms in the USA willbe established in the waters off Massachusetts and Rhode Island an area used by the CriticallyEndangered North Atlantic right whale Eubalaena glacialis Prior to 2011 little was known aboutthe use of this area by right whales We examined aerial survey data collected between 2011minus2015and 2017minus2019 to quantify right whale distribution residency demography and movements inthe region Right whale occurrence increased during the study period Since 2017 whales havebeen sighted in the area nearly every month with peak sighting rates between late winter andspring Model outputs suggest that 23 of the speciesrsquo population is present from Decemberthrough May and the mean residence time has tripled to an average of 13 d during these monthsAge and sex ratios of the individuals present in the area are similar to those of the species as awhole with adult males the most common demographic group Movement models showed thatsouthern New England is an important destination for right whales including conceptive and re -productive females and qualitative observations included animals feeding and socializing Imple-menting mitigation procedures in coordination with these findings will be crucial in lessening thepotential impacts on right whales from construction noise increased vessel traffic and habitat dis-ruption in this region

KEY WORDS Migratory species middot Alternative energy middot Aerial surveys

OPENPEN ACCESSCCESS

sectCorrections were made after publication For details seewww int-rescomabstractsesrv45c_p251-268 This corrected version August 6 2021

Endang Species Res 45 251ndash268 2021

tive conservation of migratory species requires anunderstanding of how when and which individualsuse different migratory pathways and habitats as wellas the potential stressors throughout their range

The North Atlantic right whale Eubalaena glacialis(hereafter referred to as the right whale) is a Criti-cally Endangered migratory species (Cooke 2020) Itis also one of the most endangered cetaceans world-wide with an estimated abundance of 356 individu-als (Pettis et al 2021) The population has been de -clining since 2010 (Pace et al 2017 Pettis et al 2020)due to mortality from entanglements in fixed fishinggear and vessel strikes (Corkeron et al 2018 Sharpet al 2019 Pace et al 2021) and a 40 decrease incalving (Kraus et al 2016a) including no births in2018 (Pettis et al 2020) This decrease in reproduc-tion may be attributable to chronic stress fromanthropogenic injury (van der Hoop et al 2017) andclimate-driven changes in food resources (Meyer-Gutbrod et al 2018 Record et al 2019)

Whaling records indicate that right whales once in -habited both sides of the North Atlantic (IWC Int 2001)but today the remaining population is seen almost ex-clusively along the east coast of the USA and Canadafrom Florida to the Gulf of St Lawrence with infre-quent sightings in the Gulf of Mexico and the easternNorth Atlantic (Kraus amp Rolland 2007 Firestone et al2008 Ward-Geiger et al 2011) Since 2010 their pres-ence has declined in and around once key habitats inthe Gulf of Maine and Bay of Fundy (Davies et al2015 2017) while sightings have in creased in otherareas including Cape Cod Bay Massachusetts Baythe Mid-Atlantic Bight and the Gulf of St Lawrence(Whitt et al 2013 Davis et al 2017 Mayo et al 2018Davies et al 2019 Ganley et al 2019 Charif et al2020) These shifts in distribution have been corre-lated with changes in oceanographic conditions andfood supply (Record et al 2019) and have resulted inincreased exposure to anthropo genic impacts as thewhales move into areas with little or no protectivemeasures (Davies amp Brillant 2019) The shifts haveprompted the need for in creased monitoring efforts totrack right whale distribution especially in areaswhere anthropogenic pressures are expanding

Right whale movements across habitats have con-servation implications (Brillant et al 2015) nationallyand internationally as their travel and residency pat-terns expose them to various anthropogenic activi-ties Regulations to protect right whales have beenimplemented in the USA and Canada Both countrieshave established critical habitats which are areasconsidered to contain physical and biological fea-tures essential to the speciesrsquo conservation (USA

NMFS 2016) or lsquothe habitat necessary for the survivalor recovery of a listed wildlife species and that isidentified as the speciesrsquo critical habitat in the recov-ery strategy or in an action plan for the speciesrsquo (Can-ada Brown et al 2009 Fisheries and Oceans Canada2014) Within the USA the Gulf of Maineminus GeorgesBank critical habitat is considered an important feed-ing habitat and the southeastern coast is a criticalhabitat for calving (NMFS 2016) In Canada the Bayof Fundy and Roseway Basin are critical feedinghabitats (Fisheries and Oceans Canada 2014) Theseareas were considered to be of primary importance tothe whales but feeding and calving have also beenobserved outside the established critical habitats(Patrician et al 2009 Foley et al 2011) Thus pre-dicting the speciesrsquo spatiotemporal distribution isvital in the management of human activities wherewhales and threats co-occur

Right whales were first systematically recorded insouthern New England (SNE) waters between 2011and 2015 (Kraus et al 2016b Leiter et al 2017 Stoneet al 2017) Little was known about the use of thisarea by right whales prior to this monitoring effortalthough a large influx of 102 right whales was docu-mented on 20 April 2010 by Northeast Fisheries Sci-ence Center (NEFSC) surveys (Khan et al 2011) andmodels suggested the SNE region was suitable rightwhale habitat (Pendleton et al 2012) SNE is nearother right whale habitats including the Great SouthChannel Cape Cod Bay and the mid-Atlantic migra-tory corridor (Schick et al 2009 Whitt et al 2013) con-necting the northeastern feeding grounds with thecalving grounds in the southeastern USA The 2011minus2015 monthly visual and acoustic monitoring effortfound consistent use of the area by a significant por-tion of the right whale population a strong correla-tion be tween season and presence and a peak abun-dance in the spring (Kraus et al 2016b Leiter et al2017) Over one-third of the right whale populationand 30 of the presumed living calving femalesknown at the time were documented during thesesurveys (Leiter et al 2017)

The regular presence of right whales in SNE de -serves more attention Since SNE will become one ofthe largest commercial offshore wind energy leasesalong the US east coast the consequences of the con-struction and operation are relevant to the conserva-tion of the species The effects of offshore wind devel-opment on right whales are unknown (Madsen et al2006) but this enormous development could have alocal impact on right whales at a critical time whenthey are becoming more reliant on the region (Leiter etal 2017) The construction and maintenance of hun-

252

Quintana-Rizzo et al Right whale wind energy areas

dreds of wind turbines could cause habitat changes(Wilhelmsson et al 2006) and influence oce ano graphicconditions and water column stratification (Brostroumlm2008 Paskyabi amp Fer 2012 Paskyabi 2015 Segtnan ampChristakos 2015) Both construction and maintenanceactivities may also ex pose right whales to higherlevels of vessel traffic as well as increased noise In-creased vessel traffic will result in a greater risk ofvessel strikes with right whales In addition low-fre-quency noise from large ships (20minus200 Hz) overlapsacoustic signals used by right whales (Hatch et al2012) Collectively these perturbations could affectthe use of this region by right whales as well as influ-ence their migratory movements throughout the mid-Atlantic region (Schick et al 2009)

Here we present an extended assessment of thedistribution demography residency and movementsof right whales observed in the SNE region over 2survey periods (2011minus2015 and 2017minus2019) We dis-cuss the management implications of this study andinclude recommendations for future conservationmanagement plans for this and other offshore windenergy development areas

2 MATERIALS AND METHODS

21 Field effort and right whale identifications

The study area included SNE waters from theshores of Martharsquos Vineyard and Nantucket includ-ing Nantucket Shoals Massachusetts USA to ap -proxi mately 90 km south and encompassed all thelease sites for Massachusetts and Rhode Island windenergy development Geographically the study arealies between 4050deg and 4133deg N latitude and 7140degand 6950deg W longitude (Fig 1A) The New EnglandAquarium (NEAq) conducted systematic aerial sur-veys in this region while NEFSC and the Center forCoastal Studies (CCS) conducted directed surveys toareas of right whale presence Although the level ofeffort spatial extent and configuration of the 3 sur-vey platforms varied the flights were line transectsurveys conducted from a high-winged aircraft(Cessna 337 Skymaster O-2A high-wing Cessna336 or Havilland DHC-6 Twin Otter) with 2 experi-enced observers positioned on either side of theplane Surveys were flown under visual flight rules at

253

Fig 1 Right whale critical habitats in the USA and Canada and offshore wind energy lease areas (A) Habitats studied in theanalysis of right whale movement patterns South covers the area from New York to Florida (B) Study area south of MartharsquosVineyard and Nantucket Massachusetts USA which encompasses the Rhode IslandminusMassachusetts and Massachusetts wind

energy areas BOEM Bureau of Ocean Energy Management MassCEC Massachusetts Clean Energy Center

Endang Species Res 45 251ndash268 2021

an altitude of 229 to 305 m and a target groundspeedof 185 km hminus1 Preferred environmental conditions in -cluded a minimum ceiling of 610 m visibility gt9 kmwind speed lt10 knots and Beaufort sea state le4Flight parameters (eg time latitude longitude alti-tude speed) were recorded every 2 to 5 s throughoutthe surveys and when right whales were sightedthe plane broke from the trackline and circled thewhales to obtain photographs for individual identifi-cation The plane continued the line transect surveyafter obtaining images of all right whales present inthe area Sighting and photographic data were col-lected in accordance with North Atlantic Right WhaleConsortium (NARWC) Sightings database guidelines(Kenney 2019) Individual right whales were identi-fied by distinctive callosity patterns on their headlips and chin and by scars (Kraus et al 1986) Rightwhale photographs were integrated into the NARWCIdentification database (Hamilton et al 2007) andmatched to cataloged individuals

22 Datasets and statistical analysis

The data were divided into 2 time periods 2011minus2015 (early years) and 2017minus2019 (recent years) Nosurveys were conducted by NEAq in the study areain 2016 We reanalyzed portions of the 2011minus 2015data from Leiter et al (2017) because the study areawas expanded in 2017minus2019 The NARWC provided3 datasets to support various ana lyses investigatingright whale use in SNE (NARWC 2019 2020) Data-set 1 included only right whale sightings and surveyeffort collected by the NEAq aerial surveys in thestudy area during both study periods This datasetwas used to identify clustered distribution areas andcalculate sighting rates of right whales in SNE Data-set 2 included the photographed sightings demo-graphics and behavior of identified individual rightwhales collected during systematic surveys and di -rected effort conducted by all survey teams in SNEVerification of individual right whale identificationsfor 2019 was not completed at the time of writing andwas omitted from the analysis Dataset 2 was used forresidency and demographic analyses to calculate thepercentage of right whales of the current populationsighted in SNE to summarize general behavioralactivities and to create a discovery curve of the indi-vidual right whales photographed in the study areaDiscovery curves were created to obtain a cumulativecount of distinct individuals over time and to provideinsights into whether this population was opened orclosed (Wilson et al 1999) Behavioral activities were

not quantified because the information was not al -ways collected however observations of feedingand socializing were summarized Surface or near-surface feeding was defined as an observation dur-ing which observers could see a right whale swim-ming open mouthed at or beneath the surface (Mayoet al 2018) Socializing included surface activegroups which are defined as 2 or more whales rollingand touching at the surface (Kraus amp Hatch 2001Parks et al 2007a) Dataset 3 included the sightinghistory of individual right whales observed duringsystematic surveys and directed effort in SNE by allcontributors This dataset was used to assess rightwhale movements to and from SNE and other lo -cations in the North Atlantic during the 2011minus2015and 2017minus 2018 periods Descriptive statistics werere ported as mean plusmn SE for continuous variables andN () for categorical variables

221 Distribution

Distribution and sighting rates were calculatedusing the standardized systematic survey data inDataset 1 Effort was defined as the total kilometersflown including transects circling cross-legs andtransits (Kraus et al 2016b Leiter et al 2017) Spe-cies identification confidence levels of definite (highconfidence in species identification) or probable(moderate confidence Kenney 2019) were includedin the analysis Sighting rates were calculated as thenumber of right whales sighted per 1000 km of sur-vey effort on a per-month basis to examine temporaltrends in the number of whales visiting the studyarea Monthly sighting rates across all years wereexa mined using a Kruskal-Wallis test and multipleMann-Whitney U post hoc tests were used to com-pare differences between years The 2-tailed statisti-cal tests were conducted using the SPSS 260 pack-age (2019) at a significance level of 005 Temporaland spatial analyses of sighting rates assumed thatnon-systematic periods such as circling were distrib-uted sufficiently homogeneously that a substantialbias was not incurred

A hotspot analysis was used to delineate the sea-sonal clustered distribution of right whales within thestudy area for the 2 study periods (2011minus2015 and2017minus2019) using QGIS 3106 (QGIS DevelopmentTeam 2018) The study area was divided into equallysized grids of 7 times 7 km cells Sighting rates per survey(number of right whales sighted per 1000 km) wereassigned to each corresponding cell and a hotspotanalysis was performed to test for statistically signifi-

254

Quintana-Rizzo et al Right whale wind energy areas

cant spatial clustering of right whales by seasons inthe early and recent years of the study using theQGIS Hotspot Analysis plugin (Oxoli et al 2017) Thisplugin implements the Getis-Ord Gi statistic to de-tect atypical clusters of high (hotspots) or low (cold -spots) values by looking at a cell value in the contextof its neighborsrsquo values (Getis amp Ord 1992 Oxoli et al2017) Seasons were defined as winter (DecemberminusFebruary) spring (MarchminusMay) summer (JuneminusAugust) and fall (Septemberminus November) Only sea-sonminusperiod combinations with greater than 10 rightwhale sightings were used as smaller sample sizesare considered insufficient for statistical analysis (Ott1994) Seasonal maps were compiled for each studyperiod at 3 levels of confidence (99 95 and 90)and all clusters that were within the 90 confidencelevel were considered hotspots

222 Demographics

NARWC (2020) provided sex and age class (calfjuvenile adult unknown) information for the indi-vidual right whales sighted in the study area (Dataset2) Only juvenile (defined as whales that are 1minus8 yrold) and adult (defined as whales that are 9 yr of ageor older were not seen as calves but initial sightingwas at least 8 yr prior or were known to be reproduc-tive Hamilton et al 1995) age classes were exam-ined Unknowns and dependent calves were ex -cluded because the number of sightings was toosmall (n lt 10) for statistical comparisons A G-test ofindependence was used to determine if the sex andage ratios differed from year to year and the annualage and sex ratios were compared to the correspon-ding annual ratios of the population using individualG-tests of goodness of fit with a Bonferroni correction(after Mayo et al 2018) Population ratios were calcu-lated using the minimum number of right whalespresumed alive in a given year following Knowlton etal (1994)

Since right whales were present in this region atthe time of year when conception is expected for thisspecies (Cole et al 2013) life history characteristicsof the males and females were investigated Pater-nity is determined through molecular analysis (Frasieret al 2007) and for this study genetic analysis ofknown fathers was only available for the first 3 yrBoth the proportion of reproductive females and theproportion of conceptive females compared to allidentified females present in SNE were calculated foreach year Females that had given birth in the yearsprior to or in the year of a recorded sighting were

considered reproductive (Kraus et al 2001) Femaleswere considered conceptive for a year beginning inMarch 2 yr before giving birth (Cole et al 2013) Forinstance a female first sighted with a calf anywherealong the North Atlantic between December 2014and November 2015 would be considered conceptiveduring the period 1 March 2013 through 1 March2014

223 Residence

Residence was defined as the minimum number ofdays that an individual whale was in SNE (Baracho-Neto et al 2012) To determine the residency of rightwhales in the study area maximum likelihood meth-ods were used to determine the lagged identificationrate ie the probability that an individual rightwhale will be resighted in the study area after a timelag using Dataset 2 (Whitehead 2001) This methodallows for non-random distribution of sampling effort(Whitehead 2007 2009) and the incorporation ofindividual identification data obtained during bothsystematic and directed surveys

Empirical lagged identification rate data were com-pared to a series of movement models representingclosed and open populations implemented in the pro-gram SOCPROG 29 (Whitehead 2009) (Table 1a)These models provide an estimate of the number ofvisitors in the study area based on markminus recaptureprobabilities (Whitehead 2001) SOCPROG includes 2closed population models but only one of those mod-els (A) was applied because SNE appeared to be anopen population as the discovery curve indicatedthat new right whales were identified in the studyarea over time and the 2 models provided similarresults to this dataset The following pairs of openmodels are structurally identical but parameterizeddifferently B and D C and F and E and G (Table 1)This order represents the order in which the programgenerates the results when the models are run simul-taneously All models were run simultaneously sothat the variance inflation factor could be taken fromthe most general model and applied to all of them(Whitehead 2009) Model selection was based on thelowest Akaikersquos information criterion (AIC) when thedata were overdispersed (Whitehead 2007) other-wise the lowest quasi-AIC (QAIC) was used andmodel fits were bootstrapped 100 times to generateSEs for the lagged identification rate estimates

The lagged identification rate was calculated fromthe best-fit model applied to sighting data collectedfrom December to May the period when previous

255

Endang Species Res 45 251ndash268 2021

studies identified a high right whale presence in thearea (Kraus et al 2016b Leiter et al 2017) Residencywas estimated for the 2 time periods (2011minus2015 and2017minus2018) to determine if it changed over time Thelagged identification rates were calculated andmodels fitted for males and females separately toinvestigate whether the sexes exhibited differentresidency patterns The number of right whale iden-tifications for summer and fall was too low to calcu-late a separate lagged identification rate but the per-centages of individual right whales sighted in thesummer and fall were calculated These models havebeen used for cetaceans (eg Wimmer amp Whitehead2004 Dinis et al 2016 Chabanne et al 2017) andother migratory marine megafauna (eg manta raysDeakos et al 2011 whale sharks McKinney et al2017 McCoy et al 2018)

224 Movements

Dataset 3 was used to estimate the seasonal transi-tion probabilities between SNE and other areas forboth study periods The analysis was limited to themovements between SNE and no more than 4 areas

to ensure precise estimates given by the small num-ber of habitat comparisons and the high number ofidentified individuals moving among areas (White-head 2009) The areas followed Brillant et al (2015)and included from north to south the Gulf of StLawrence Bay of Fundy Gulf of Maine (includingthe Columbia and Jeffreys ledges and Jordan Basin)Cape Cod Bay Great South ChannelminusGeorges Bankand the South (from New York to Florida) (Fig 1B)The mid-Atlantic was combined with adjacent areasto the south to increase the sample size

Transition probabilities were calculated using apara meterized Markov movement model inSOCPROG 29 (Whitehead 2009) This population-scale behavior model uses the locations and eachtime unit of photographically identified individuals toestimate the probability of moving from one area toanother at a time lag (Whitehead 2001) This modelcan be used with identifications that are not distrib-uted randomly or uniformly in space or time and thathave no independent measure of effort (Whitehead2001) The small number (n lt 10) of seasonal rightwhale identifications in SNE in fall and summer2011minus 2015 did not permit the estimation of transitionprobabilities for those seasons A 30 d lag was used

256

aModel Model type and parameters

A Closed (1a1 = N or number of visitors)

B Emigrationmortality (a1 = emigration rate 1a2 = N)

C Emigration + reimmigration (a1 = emigration rate a2(a2 + a3) = proportion of population in study area atany time)

D Emigrationmortality (a1 = N a2 = mean residence time)

E Emigration + reimmigration + mortality

F Emigration + reimmigration (a1 = N a2 = mean time in study area a3 = mean time out of study area)

G Emigration + reimmigration + mortality (a1 = N a2 = mean time in study area a3 = mean time out of studyarea a4 = mortality rate)

bModel All Female Male AIC QAIC AIC QAIC AIC QAIC 2011minus2015 2017minus2018 2011minus2015 2017minus2018 2011minus2015 2017minus2018

A 35732 149084 15468 50423 35750 49668B 35630 147694 15447 50488 89158 48730C 36039 145885a 15674 49626a 35694a 47989a

D 35630 147694 15447 50489 35806 48730E 35979 146659 15770 49796 35906 48663F 35120a 145885a 15340a 49626a 35694a 47989a

G 35289 146084 52378 50268 35872 48291

aBest-fit model (with lowest AIC or QAIC value)

Table 1 (a) Models and parameters and (b) fits and comparison for lagged identification rate of all right whales females and males in southern New England during 2 time periods AIC Akaikersquos information criterion QAIC quasi-AIC

Quintana-Rizzo et al Right whale wind energy areas

based on the assumption that an identified rightwhale in any location could reach any of these otherhabitats within this interval (Brillant et al 2015Davies et al 2015) during the season of interestBack-and-forth movements of right whales betweensouthern New England and nearby areas wereexplored by examining the sighting histories of indi-vidual right whales

3 RESULTS

31 Field effort right whale identificationsand behavioral activities

The combined survey effort in southern New Eng-land covered 111 440 km between March 2011 andDecember 2019 (Table 2) The annual tally of rightwhales reported (not unique whale identifications)from all sightings varied between 28 and 418 (144 plusmn49 whales) A total of 327 unique right whales wereidentified with a mean number of 9 identificationsper survey day At least 16 of these whales were con-firmed dead according to NARWC as of the begin-ning of December 2020 The discovery curve showedan increasing trend in the number of new individualssighted with no clear plateau signal (Fig 2) and bythe end of 2019 87 of the current population hadbeen sighted in SNE throughout the study periodThe discovery curve had a steep slope during the2011minus 2015 surveys and was even steeper in 2017minus2018 suggesting an open population or that sight-ings in the area were underestimated Feeding wasrecorded on more occasions (n = 190 occasions) thansocializing (n = 59 occasions) Feeding was observedin all seasons and years whereas social behaviorswere observed mainly in the winter and spring andwere not observed in 2011 and 2017

32 Datasets and statistical analysis

321 Distribution

Sighting rates varied through time suggesting thatright whales have become more common in recentyears and that their presence now extends beyondthe DecemberminusMay period in SNE No right whaleswere reported in 2011 in Dataset 1 but the NEAqsurveys did not start until October that year Sightingrates varied in most other years (Fig 3 Kruskal-Wallis test = 2067 df = 6 p = 0002) Pairwise com-parisons showed that the sighting rates of right

whales were not significantly different among theearly years of the study and the sighting rates ofmost of those years were lower than those of recentyears (Fig 3) Sighting rates were not statistically dif-ferent in 2015 2017 and 2018 (Fig 3) Right whalesightings by month were highest from January toApril during the early years of the study but inrecent years right whales were sighted in mostmonths of the year with notably high sighting ratesin December 2018 and August 2019 (Fig 4)

The seasonal clustered distribution of right whalesvaried in space and time and extended into wind

257

Year Tally of Unique of NEAq NEFSC CCS right ID population (km) (km) (km) whales plusmn SE

2011 83 53 11 plusmn 1 4279 2455 3272012 28 22 5 plusmn 1 16 042 1471 minus2013 32 20 4 plusmn 1 12 890 779 minus2014 44 43 9 plusmn 1 17 279 1763 minus2015 86 53 11 plusmn 1 9594 6761 3572017 214 122 29 plusmn 2 18 867 2456 minus2018 418 202 53 plusmn 2 11 295 9732 minus2019 250 NA NC 20729 NA minus

Table 2 Total tally of right whales recorded in all sightings(no ID included) unique ID population percentage sightedin relation to the general right whale population (based onPace et al 2017 and Pettis et al 2021 updated population es-timates) and annual survey effort (km) in southern NewEngland waters by main data contributors NEAq NewEngland Aquarium NEFSC Northeast Fisheries ScienceCenter CCS Center for Coastal Studies NA not availableat the time of the data request NC not calculated (number

of unique IDs not available) (ndash) no data

Fig 2 Discovery curve for the number of uniquely identifiedindividual right whales sighted in southern New EnglandThe slope of the curve indicates an open population wherenot all individuals have been sampled No field effort was

conducted in 2016

Endang Species Res 45 251ndash268 2021258

A Mann-Whitney U-test statistical values Year 2012 2013 2014 2015 2017 2018 2019 2012 4950 5600 1600 2650 1800 750 2013 096 5600 1500 2750 1900 1050 2014 075 075 2200 4100 3000 1000 2015 021 017 034 2700 1800 900 2017 004 004 010 095 4300 1850 2018 001 001 004 039 039 2400 2019 0002 0006 0002 011 003 015

p-v

alue

s

2011

Sig

htin

g ra

teno

of r

ight

wha

les

per

100

0 km

of s

urve

y

40

30

20

10

02012 2013 2014 2015 2016 2017 2018 2019

B

Fig 3 (A) Mann-Whitney U-test comparisons and (B) central tendency and variability of sighting rates of right whales Noright whale sightings were reported in 2011 and no field effort was conducted in 2016 in Dataset 1 (sightings and survey effortcollected during aerial surveys conducted by the New England Aquarium) The solid line drawn across each box representsthe median sighting rate of that year The lower boundary is the 25th percentile and the upper boundary is the 75th percentileof a box Lines on the top and bottom of each box represent the largest and smallest frequency sighting rates respectively

excluding outliers (o) and extreme values (Δ) p lt 005

Fig 4 Monthly sighting rates of right whales and monthlyaerial surveys conducted in the study area in Dataset 1(sightings and survey effort collected during aerial surveysconducted by the New England Aquarium) Sighting rate isdefined as the number of right whales per 1000 km of surveyThe number of IDs including resightings is included forthose months in which IDs were available in Dataset 2 (IDscollected by all survey teams) The 2019 IDs were not avail-

able at the time of the data request

Quintana-Rizzo et al Right whale wind energy areas

energy lease sites In the 2011minus2015 winters rightwhale sightings increased in the study area and weremore concentrated in the northeastern wind energyareas and the southern portion of Nantucket Shoals(Fig 5A) However in the 2017minus2019 winters thesightings spanned to the southeastern portion of theshoals (Fig 5B) In the spring right whale distribu-tion shifted to the west in both study periodsalthough in the early years their distribution was fur-ther south of Nantucket (Fig 5CD) Summer sight-ings were only recorded during the 2017minus2019period with right whales sighted in nearshore watersoff Nantucket and along Nantucket Shoals (Fig 5E)

322 Demographics

The ratio of adults to juveniles in SNE was the sameas in the population as a whole during the studyAdult whales were observed significantly more thanjuveniles with an annual mean of 70 adults and30 juveniles The adultjuvenile ratio was signifi-cantly different from year to year (G = 2061 χ2 df = 6p lt 0002) but the annual ratios were not significantlydifferent from the yearly population age ratios(Table 3) indicating that the age ratio of the whalesvisiting the study area followed the age ratio of thepopulation Sex was confirmed for 93 of the identifi-

259

Fig 5 Hotspot analysis of right whale seasonal distribution in the study area (AC 2011ndash2015 BDE 2017ndash2019) with hotspotsbased on significantly higher values than surrounding areas No coldspots were identified Wind energy area lease zones are

identified by numbers Additional details of the study area are shown in Fig 1

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Quintana-Rizzo et al Right whale wind energy areas

dreds of wind turbines could cause habitat changes(Wilhelmsson et al 2006) and influence oce ano graphicconditions and water column stratification (Brostroumlm2008 Paskyabi amp Fer 2012 Paskyabi 2015 Segtnan ampChristakos 2015) Both construction and maintenanceactivities may also ex pose right whales to higherlevels of vessel traffic as well as increased noise In-creased vessel traffic will result in a greater risk ofvessel strikes with right whales In addition low-fre-quency noise from large ships (20minus200 Hz) overlapsacoustic signals used by right whales (Hatch et al2012) Collectively these perturbations could affectthe use of this region by right whales as well as influ-ence their migratory movements throughout the mid-Atlantic region (Schick et al 2009)

Here we present an extended assessment of thedistribution demography residency and movementsof right whales observed in the SNE region over 2survey periods (2011minus2015 and 2017minus2019) We dis-cuss the management implications of this study andinclude recommendations for future conservationmanagement plans for this and other offshore windenergy development areas

2 MATERIALS AND METHODS

21 Field effort and right whale identifications

The study area included SNE waters from theshores of Martharsquos Vineyard and Nantucket includ-ing Nantucket Shoals Massachusetts USA to ap -proxi mately 90 km south and encompassed all thelease sites for Massachusetts and Rhode Island windenergy development Geographically the study arealies between 4050deg and 4133deg N latitude and 7140degand 6950deg W longitude (Fig 1A) The New EnglandAquarium (NEAq) conducted systematic aerial sur-veys in this region while NEFSC and the Center forCoastal Studies (CCS) conducted directed surveys toareas of right whale presence Although the level ofeffort spatial extent and configuration of the 3 sur-vey platforms varied the flights were line transectsurveys conducted from a high-winged aircraft(Cessna 337 Skymaster O-2A high-wing Cessna336 or Havilland DHC-6 Twin Otter) with 2 experi-enced observers positioned on either side of theplane Surveys were flown under visual flight rules at

253

Fig 1 Right whale critical habitats in the USA and Canada and offshore wind energy lease areas (A) Habitats studied in theanalysis of right whale movement patterns South covers the area from New York to Florida (B) Study area south of MartharsquosVineyard and Nantucket Massachusetts USA which encompasses the Rhode IslandminusMassachusetts and Massachusetts wind

energy areas BOEM Bureau of Ocean Energy Management MassCEC Massachusetts Clean Energy Center

Endang Species Res 45 251ndash268 2021

an altitude of 229 to 305 m and a target groundspeedof 185 km hminus1 Preferred environmental conditions in -cluded a minimum ceiling of 610 m visibility gt9 kmwind speed lt10 knots and Beaufort sea state le4Flight parameters (eg time latitude longitude alti-tude speed) were recorded every 2 to 5 s throughoutthe surveys and when right whales were sightedthe plane broke from the trackline and circled thewhales to obtain photographs for individual identifi-cation The plane continued the line transect surveyafter obtaining images of all right whales present inthe area Sighting and photographic data were col-lected in accordance with North Atlantic Right WhaleConsortium (NARWC) Sightings database guidelines(Kenney 2019) Individual right whales were identi-fied by distinctive callosity patterns on their headlips and chin and by scars (Kraus et al 1986) Rightwhale photographs were integrated into the NARWCIdentification database (Hamilton et al 2007) andmatched to cataloged individuals

22 Datasets and statistical analysis

The data were divided into 2 time periods 2011minus2015 (early years) and 2017minus2019 (recent years) Nosurveys were conducted by NEAq in the study areain 2016 We reanalyzed portions of the 2011minus 2015data from Leiter et al (2017) because the study areawas expanded in 2017minus2019 The NARWC provided3 datasets to support various ana lyses investigatingright whale use in SNE (NARWC 2019 2020) Data-set 1 included only right whale sightings and surveyeffort collected by the NEAq aerial surveys in thestudy area during both study periods This datasetwas used to identify clustered distribution areas andcalculate sighting rates of right whales in SNE Data-set 2 included the photographed sightings demo-graphics and behavior of identified individual rightwhales collected during systematic surveys and di -rected effort conducted by all survey teams in SNEVerification of individual right whale identificationsfor 2019 was not completed at the time of writing andwas omitted from the analysis Dataset 2 was used forresidency and demographic analyses to calculate thepercentage of right whales of the current populationsighted in SNE to summarize general behavioralactivities and to create a discovery curve of the indi-vidual right whales photographed in the study areaDiscovery curves were created to obtain a cumulativecount of distinct individuals over time and to provideinsights into whether this population was opened orclosed (Wilson et al 1999) Behavioral activities were

not quantified because the information was not al -ways collected however observations of feedingand socializing were summarized Surface or near-surface feeding was defined as an observation dur-ing which observers could see a right whale swim-ming open mouthed at or beneath the surface (Mayoet al 2018) Socializing included surface activegroups which are defined as 2 or more whales rollingand touching at the surface (Kraus amp Hatch 2001Parks et al 2007a) Dataset 3 included the sightinghistory of individual right whales observed duringsystematic surveys and directed effort in SNE by allcontributors This dataset was used to assess rightwhale movements to and from SNE and other lo -cations in the North Atlantic during the 2011minus2015and 2017minus 2018 periods Descriptive statistics werere ported as mean plusmn SE for continuous variables andN () for categorical variables

221 Distribution

Distribution and sighting rates were calculatedusing the standardized systematic survey data inDataset 1 Effort was defined as the total kilometersflown including transects circling cross-legs andtransits (Kraus et al 2016b Leiter et al 2017) Spe-cies identification confidence levels of definite (highconfidence in species identification) or probable(moderate confidence Kenney 2019) were includedin the analysis Sighting rates were calculated as thenumber of right whales sighted per 1000 km of sur-vey effort on a per-month basis to examine temporaltrends in the number of whales visiting the studyarea Monthly sighting rates across all years wereexa mined using a Kruskal-Wallis test and multipleMann-Whitney U post hoc tests were used to com-pare differences between years The 2-tailed statisti-cal tests were conducted using the SPSS 260 pack-age (2019) at a significance level of 005 Temporaland spatial analyses of sighting rates assumed thatnon-systematic periods such as circling were distrib-uted sufficiently homogeneously that a substantialbias was not incurred

A hotspot analysis was used to delineate the sea-sonal clustered distribution of right whales within thestudy area for the 2 study periods (2011minus2015 and2017minus2019) using QGIS 3106 (QGIS DevelopmentTeam 2018) The study area was divided into equallysized grids of 7 times 7 km cells Sighting rates per survey(number of right whales sighted per 1000 km) wereassigned to each corresponding cell and a hotspotanalysis was performed to test for statistically signifi-

254

Quintana-Rizzo et al Right whale wind energy areas

cant spatial clustering of right whales by seasons inthe early and recent years of the study using theQGIS Hotspot Analysis plugin (Oxoli et al 2017) Thisplugin implements the Getis-Ord Gi statistic to de-tect atypical clusters of high (hotspots) or low (cold -spots) values by looking at a cell value in the contextof its neighborsrsquo values (Getis amp Ord 1992 Oxoli et al2017) Seasons were defined as winter (DecemberminusFebruary) spring (MarchminusMay) summer (JuneminusAugust) and fall (Septemberminus November) Only sea-sonminusperiod combinations with greater than 10 rightwhale sightings were used as smaller sample sizesare considered insufficient for statistical analysis (Ott1994) Seasonal maps were compiled for each studyperiod at 3 levels of confidence (99 95 and 90)and all clusters that were within the 90 confidencelevel were considered hotspots

222 Demographics

NARWC (2020) provided sex and age class (calfjuvenile adult unknown) information for the indi-vidual right whales sighted in the study area (Dataset2) Only juvenile (defined as whales that are 1minus8 yrold) and adult (defined as whales that are 9 yr of ageor older were not seen as calves but initial sightingwas at least 8 yr prior or were known to be reproduc-tive Hamilton et al 1995) age classes were exam-ined Unknowns and dependent calves were ex -cluded because the number of sightings was toosmall (n lt 10) for statistical comparisons A G-test ofindependence was used to determine if the sex andage ratios differed from year to year and the annualage and sex ratios were compared to the correspon-ding annual ratios of the population using individualG-tests of goodness of fit with a Bonferroni correction(after Mayo et al 2018) Population ratios were calcu-lated using the minimum number of right whalespresumed alive in a given year following Knowlton etal (1994)

Since right whales were present in this region atthe time of year when conception is expected for thisspecies (Cole et al 2013) life history characteristicsof the males and females were investigated Pater-nity is determined through molecular analysis (Frasieret al 2007) and for this study genetic analysis ofknown fathers was only available for the first 3 yrBoth the proportion of reproductive females and theproportion of conceptive females compared to allidentified females present in SNE were calculated foreach year Females that had given birth in the yearsprior to or in the year of a recorded sighting were

considered reproductive (Kraus et al 2001) Femaleswere considered conceptive for a year beginning inMarch 2 yr before giving birth (Cole et al 2013) Forinstance a female first sighted with a calf anywherealong the North Atlantic between December 2014and November 2015 would be considered conceptiveduring the period 1 March 2013 through 1 March2014

223 Residence

Residence was defined as the minimum number ofdays that an individual whale was in SNE (Baracho-Neto et al 2012) To determine the residency of rightwhales in the study area maximum likelihood meth-ods were used to determine the lagged identificationrate ie the probability that an individual rightwhale will be resighted in the study area after a timelag using Dataset 2 (Whitehead 2001) This methodallows for non-random distribution of sampling effort(Whitehead 2007 2009) and the incorporation ofindividual identification data obtained during bothsystematic and directed surveys

Empirical lagged identification rate data were com-pared to a series of movement models representingclosed and open populations implemented in the pro-gram SOCPROG 29 (Whitehead 2009) (Table 1a)These models provide an estimate of the number ofvisitors in the study area based on markminus recaptureprobabilities (Whitehead 2001) SOCPROG includes 2closed population models but only one of those mod-els (A) was applied because SNE appeared to be anopen population as the discovery curve indicatedthat new right whales were identified in the studyarea over time and the 2 models provided similarresults to this dataset The following pairs of openmodels are structurally identical but parameterizeddifferently B and D C and F and E and G (Table 1)This order represents the order in which the programgenerates the results when the models are run simul-taneously All models were run simultaneously sothat the variance inflation factor could be taken fromthe most general model and applied to all of them(Whitehead 2009) Model selection was based on thelowest Akaikersquos information criterion (AIC) when thedata were overdispersed (Whitehead 2007) other-wise the lowest quasi-AIC (QAIC) was used andmodel fits were bootstrapped 100 times to generateSEs for the lagged identification rate estimates

The lagged identification rate was calculated fromthe best-fit model applied to sighting data collectedfrom December to May the period when previous

255

Endang Species Res 45 251ndash268 2021

studies identified a high right whale presence in thearea (Kraus et al 2016b Leiter et al 2017) Residencywas estimated for the 2 time periods (2011minus2015 and2017minus2018) to determine if it changed over time Thelagged identification rates were calculated andmodels fitted for males and females separately toinvestigate whether the sexes exhibited differentresidency patterns The number of right whale iden-tifications for summer and fall was too low to calcu-late a separate lagged identification rate but the per-centages of individual right whales sighted in thesummer and fall were calculated These models havebeen used for cetaceans (eg Wimmer amp Whitehead2004 Dinis et al 2016 Chabanne et al 2017) andother migratory marine megafauna (eg manta raysDeakos et al 2011 whale sharks McKinney et al2017 McCoy et al 2018)

224 Movements

Dataset 3 was used to estimate the seasonal transi-tion probabilities between SNE and other areas forboth study periods The analysis was limited to themovements between SNE and no more than 4 areas

to ensure precise estimates given by the small num-ber of habitat comparisons and the high number ofidentified individuals moving among areas (White-head 2009) The areas followed Brillant et al (2015)and included from north to south the Gulf of StLawrence Bay of Fundy Gulf of Maine (includingthe Columbia and Jeffreys ledges and Jordan Basin)Cape Cod Bay Great South ChannelminusGeorges Bankand the South (from New York to Florida) (Fig 1B)The mid-Atlantic was combined with adjacent areasto the south to increase the sample size

Transition probabilities were calculated using apara meterized Markov movement model inSOCPROG 29 (Whitehead 2009) This population-scale behavior model uses the locations and eachtime unit of photographically identified individuals toestimate the probability of moving from one area toanother at a time lag (Whitehead 2001) This modelcan be used with identifications that are not distrib-uted randomly or uniformly in space or time and thathave no independent measure of effort (Whitehead2001) The small number (n lt 10) of seasonal rightwhale identifications in SNE in fall and summer2011minus 2015 did not permit the estimation of transitionprobabilities for those seasons A 30 d lag was used

256

aModel Model type and parameters

A Closed (1a1 = N or number of visitors)

B Emigrationmortality (a1 = emigration rate 1a2 = N)

C Emigration + reimmigration (a1 = emigration rate a2(a2 + a3) = proportion of population in study area atany time)

D Emigrationmortality (a1 = N a2 = mean residence time)

E Emigration + reimmigration + mortality

F Emigration + reimmigration (a1 = N a2 = mean time in study area a3 = mean time out of study area)

G Emigration + reimmigration + mortality (a1 = N a2 = mean time in study area a3 = mean time out of studyarea a4 = mortality rate)

bModel All Female Male AIC QAIC AIC QAIC AIC QAIC 2011minus2015 2017minus2018 2011minus2015 2017minus2018 2011minus2015 2017minus2018

A 35732 149084 15468 50423 35750 49668B 35630 147694 15447 50488 89158 48730C 36039 145885a 15674 49626a 35694a 47989a

D 35630 147694 15447 50489 35806 48730E 35979 146659 15770 49796 35906 48663F 35120a 145885a 15340a 49626a 35694a 47989a

G 35289 146084 52378 50268 35872 48291

aBest-fit model (with lowest AIC or QAIC value)

Table 1 (a) Models and parameters and (b) fits and comparison for lagged identification rate of all right whales females and males in southern New England during 2 time periods AIC Akaikersquos information criterion QAIC quasi-AIC

Quintana-Rizzo et al Right whale wind energy areas

based on the assumption that an identified rightwhale in any location could reach any of these otherhabitats within this interval (Brillant et al 2015Davies et al 2015) during the season of interestBack-and-forth movements of right whales betweensouthern New England and nearby areas wereexplored by examining the sighting histories of indi-vidual right whales

3 RESULTS

31 Field effort right whale identificationsand behavioral activities

The combined survey effort in southern New Eng-land covered 111 440 km between March 2011 andDecember 2019 (Table 2) The annual tally of rightwhales reported (not unique whale identifications)from all sightings varied between 28 and 418 (144 plusmn49 whales) A total of 327 unique right whales wereidentified with a mean number of 9 identificationsper survey day At least 16 of these whales were con-firmed dead according to NARWC as of the begin-ning of December 2020 The discovery curve showedan increasing trend in the number of new individualssighted with no clear plateau signal (Fig 2) and bythe end of 2019 87 of the current population hadbeen sighted in SNE throughout the study periodThe discovery curve had a steep slope during the2011minus 2015 surveys and was even steeper in 2017minus2018 suggesting an open population or that sight-ings in the area were underestimated Feeding wasrecorded on more occasions (n = 190 occasions) thansocializing (n = 59 occasions) Feeding was observedin all seasons and years whereas social behaviorswere observed mainly in the winter and spring andwere not observed in 2011 and 2017

32 Datasets and statistical analysis

321 Distribution

Sighting rates varied through time suggesting thatright whales have become more common in recentyears and that their presence now extends beyondthe DecemberminusMay period in SNE No right whaleswere reported in 2011 in Dataset 1 but the NEAqsurveys did not start until October that year Sightingrates varied in most other years (Fig 3 Kruskal-Wallis test = 2067 df = 6 p = 0002) Pairwise com-parisons showed that the sighting rates of right

whales were not significantly different among theearly years of the study and the sighting rates ofmost of those years were lower than those of recentyears (Fig 3) Sighting rates were not statistically dif-ferent in 2015 2017 and 2018 (Fig 3) Right whalesightings by month were highest from January toApril during the early years of the study but inrecent years right whales were sighted in mostmonths of the year with notably high sighting ratesin December 2018 and August 2019 (Fig 4)

The seasonal clustered distribution of right whalesvaried in space and time and extended into wind

257

Year Tally of Unique of NEAq NEFSC CCS right ID population (km) (km) (km) whales plusmn SE

2011 83 53 11 plusmn 1 4279 2455 3272012 28 22 5 plusmn 1 16 042 1471 minus2013 32 20 4 plusmn 1 12 890 779 minus2014 44 43 9 plusmn 1 17 279 1763 minus2015 86 53 11 plusmn 1 9594 6761 3572017 214 122 29 plusmn 2 18 867 2456 minus2018 418 202 53 plusmn 2 11 295 9732 minus2019 250 NA NC 20729 NA minus

Table 2 Total tally of right whales recorded in all sightings(no ID included) unique ID population percentage sightedin relation to the general right whale population (based onPace et al 2017 and Pettis et al 2021 updated population es-timates) and annual survey effort (km) in southern NewEngland waters by main data contributors NEAq NewEngland Aquarium NEFSC Northeast Fisheries ScienceCenter CCS Center for Coastal Studies NA not availableat the time of the data request NC not calculated (number

of unique IDs not available) (ndash) no data

Fig 2 Discovery curve for the number of uniquely identifiedindividual right whales sighted in southern New EnglandThe slope of the curve indicates an open population wherenot all individuals have been sampled No field effort was

conducted in 2016

Endang Species Res 45 251ndash268 2021258

A Mann-Whitney U-test statistical values Year 2012 2013 2014 2015 2017 2018 2019 2012 4950 5600 1600 2650 1800 750 2013 096 5600 1500 2750 1900 1050 2014 075 075 2200 4100 3000 1000 2015 021 017 034 2700 1800 900 2017 004 004 010 095 4300 1850 2018 001 001 004 039 039 2400 2019 0002 0006 0002 011 003 015

p-v

alue

s

2011

Sig

htin

g ra

teno

of r

ight

wha

les

per

100

0 km

of s

urve

y

40

30

20

10

02012 2013 2014 2015 2016 2017 2018 2019

B

Fig 3 (A) Mann-Whitney U-test comparisons and (B) central tendency and variability of sighting rates of right whales Noright whale sightings were reported in 2011 and no field effort was conducted in 2016 in Dataset 1 (sightings and survey effortcollected during aerial surveys conducted by the New England Aquarium) The solid line drawn across each box representsthe median sighting rate of that year The lower boundary is the 25th percentile and the upper boundary is the 75th percentileof a box Lines on the top and bottom of each box represent the largest and smallest frequency sighting rates respectively

excluding outliers (o) and extreme values (Δ) p lt 005

Fig 4 Monthly sighting rates of right whales and monthlyaerial surveys conducted in the study area in Dataset 1(sightings and survey effort collected during aerial surveysconducted by the New England Aquarium) Sighting rate isdefined as the number of right whales per 1000 km of surveyThe number of IDs including resightings is included forthose months in which IDs were available in Dataset 2 (IDscollected by all survey teams) The 2019 IDs were not avail-

able at the time of the data request

Quintana-Rizzo et al Right whale wind energy areas

energy lease sites In the 2011minus2015 winters rightwhale sightings increased in the study area and weremore concentrated in the northeastern wind energyareas and the southern portion of Nantucket Shoals(Fig 5A) However in the 2017minus2019 winters thesightings spanned to the southeastern portion of theshoals (Fig 5B) In the spring right whale distribu-tion shifted to the west in both study periodsalthough in the early years their distribution was fur-ther south of Nantucket (Fig 5CD) Summer sight-ings were only recorded during the 2017minus2019period with right whales sighted in nearshore watersoff Nantucket and along Nantucket Shoals (Fig 5E)

322 Demographics

The ratio of adults to juveniles in SNE was the sameas in the population as a whole during the studyAdult whales were observed significantly more thanjuveniles with an annual mean of 70 adults and30 juveniles The adultjuvenile ratio was signifi-cantly different from year to year (G = 2061 χ2 df = 6p lt 0002) but the annual ratios were not significantlydifferent from the yearly population age ratios(Table 3) indicating that the age ratio of the whalesvisiting the study area followed the age ratio of thepopulation Sex was confirmed for 93 of the identifi-

259

Fig 5 Hotspot analysis of right whale seasonal distribution in the study area (AC 2011ndash2015 BDE 2017ndash2019) with hotspotsbased on significantly higher values than surrounding areas No coldspots were identified Wind energy area lease zones are

identified by numbers Additional details of the study area are shown in Fig 1

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Endang Species Res 45 251ndash268 2021

an altitude of 229 to 305 m and a target groundspeedof 185 km hminus1 Preferred environmental conditions in -cluded a minimum ceiling of 610 m visibility gt9 kmwind speed lt10 knots and Beaufort sea state le4Flight parameters (eg time latitude longitude alti-tude speed) were recorded every 2 to 5 s throughoutthe surveys and when right whales were sightedthe plane broke from the trackline and circled thewhales to obtain photographs for individual identifi-cation The plane continued the line transect surveyafter obtaining images of all right whales present inthe area Sighting and photographic data were col-lected in accordance with North Atlantic Right WhaleConsortium (NARWC) Sightings database guidelines(Kenney 2019) Individual right whales were identi-fied by distinctive callosity patterns on their headlips and chin and by scars (Kraus et al 1986) Rightwhale photographs were integrated into the NARWCIdentification database (Hamilton et al 2007) andmatched to cataloged individuals

22 Datasets and statistical analysis

The data were divided into 2 time periods 2011minus2015 (early years) and 2017minus2019 (recent years) Nosurveys were conducted by NEAq in the study areain 2016 We reanalyzed portions of the 2011minus 2015data from Leiter et al (2017) because the study areawas expanded in 2017minus2019 The NARWC provided3 datasets to support various ana lyses investigatingright whale use in SNE (NARWC 2019 2020) Data-set 1 included only right whale sightings and surveyeffort collected by the NEAq aerial surveys in thestudy area during both study periods This datasetwas used to identify clustered distribution areas andcalculate sighting rates of right whales in SNE Data-set 2 included the photographed sightings demo-graphics and behavior of identified individual rightwhales collected during systematic surveys and di -rected effort conducted by all survey teams in SNEVerification of individual right whale identificationsfor 2019 was not completed at the time of writing andwas omitted from the analysis Dataset 2 was used forresidency and demographic analyses to calculate thepercentage of right whales of the current populationsighted in SNE to summarize general behavioralactivities and to create a discovery curve of the indi-vidual right whales photographed in the study areaDiscovery curves were created to obtain a cumulativecount of distinct individuals over time and to provideinsights into whether this population was opened orclosed (Wilson et al 1999) Behavioral activities were

not quantified because the information was not al -ways collected however observations of feedingand socializing were summarized Surface or near-surface feeding was defined as an observation dur-ing which observers could see a right whale swim-ming open mouthed at or beneath the surface (Mayoet al 2018) Socializing included surface activegroups which are defined as 2 or more whales rollingand touching at the surface (Kraus amp Hatch 2001Parks et al 2007a) Dataset 3 included the sightinghistory of individual right whales observed duringsystematic surveys and directed effort in SNE by allcontributors This dataset was used to assess rightwhale movements to and from SNE and other lo -cations in the North Atlantic during the 2011minus2015and 2017minus 2018 periods Descriptive statistics werere ported as mean plusmn SE for continuous variables andN () for categorical variables

221 Distribution

Distribution and sighting rates were calculatedusing the standardized systematic survey data inDataset 1 Effort was defined as the total kilometersflown including transects circling cross-legs andtransits (Kraus et al 2016b Leiter et al 2017) Spe-cies identification confidence levels of definite (highconfidence in species identification) or probable(moderate confidence Kenney 2019) were includedin the analysis Sighting rates were calculated as thenumber of right whales sighted per 1000 km of sur-vey effort on a per-month basis to examine temporaltrends in the number of whales visiting the studyarea Monthly sighting rates across all years wereexa mined using a Kruskal-Wallis test and multipleMann-Whitney U post hoc tests were used to com-pare differences between years The 2-tailed statisti-cal tests were conducted using the SPSS 260 pack-age (2019) at a significance level of 005 Temporaland spatial analyses of sighting rates assumed thatnon-systematic periods such as circling were distrib-uted sufficiently homogeneously that a substantialbias was not incurred

A hotspot analysis was used to delineate the sea-sonal clustered distribution of right whales within thestudy area for the 2 study periods (2011minus2015 and2017minus2019) using QGIS 3106 (QGIS DevelopmentTeam 2018) The study area was divided into equallysized grids of 7 times 7 km cells Sighting rates per survey(number of right whales sighted per 1000 km) wereassigned to each corresponding cell and a hotspotanalysis was performed to test for statistically signifi-

254

Quintana-Rizzo et al Right whale wind energy areas

cant spatial clustering of right whales by seasons inthe early and recent years of the study using theQGIS Hotspot Analysis plugin (Oxoli et al 2017) Thisplugin implements the Getis-Ord Gi statistic to de-tect atypical clusters of high (hotspots) or low (cold -spots) values by looking at a cell value in the contextof its neighborsrsquo values (Getis amp Ord 1992 Oxoli et al2017) Seasons were defined as winter (DecemberminusFebruary) spring (MarchminusMay) summer (JuneminusAugust) and fall (Septemberminus November) Only sea-sonminusperiod combinations with greater than 10 rightwhale sightings were used as smaller sample sizesare considered insufficient for statistical analysis (Ott1994) Seasonal maps were compiled for each studyperiod at 3 levels of confidence (99 95 and 90)and all clusters that were within the 90 confidencelevel were considered hotspots

222 Demographics

NARWC (2020) provided sex and age class (calfjuvenile adult unknown) information for the indi-vidual right whales sighted in the study area (Dataset2) Only juvenile (defined as whales that are 1minus8 yrold) and adult (defined as whales that are 9 yr of ageor older were not seen as calves but initial sightingwas at least 8 yr prior or were known to be reproduc-tive Hamilton et al 1995) age classes were exam-ined Unknowns and dependent calves were ex -cluded because the number of sightings was toosmall (n lt 10) for statistical comparisons A G-test ofindependence was used to determine if the sex andage ratios differed from year to year and the annualage and sex ratios were compared to the correspon-ding annual ratios of the population using individualG-tests of goodness of fit with a Bonferroni correction(after Mayo et al 2018) Population ratios were calcu-lated using the minimum number of right whalespresumed alive in a given year following Knowlton etal (1994)

Since right whales were present in this region atthe time of year when conception is expected for thisspecies (Cole et al 2013) life history characteristicsof the males and females were investigated Pater-nity is determined through molecular analysis (Frasieret al 2007) and for this study genetic analysis ofknown fathers was only available for the first 3 yrBoth the proportion of reproductive females and theproportion of conceptive females compared to allidentified females present in SNE were calculated foreach year Females that had given birth in the yearsprior to or in the year of a recorded sighting were

considered reproductive (Kraus et al 2001) Femaleswere considered conceptive for a year beginning inMarch 2 yr before giving birth (Cole et al 2013) Forinstance a female first sighted with a calf anywherealong the North Atlantic between December 2014and November 2015 would be considered conceptiveduring the period 1 March 2013 through 1 March2014

223 Residence

Residence was defined as the minimum number ofdays that an individual whale was in SNE (Baracho-Neto et al 2012) To determine the residency of rightwhales in the study area maximum likelihood meth-ods were used to determine the lagged identificationrate ie the probability that an individual rightwhale will be resighted in the study area after a timelag using Dataset 2 (Whitehead 2001) This methodallows for non-random distribution of sampling effort(Whitehead 2007 2009) and the incorporation ofindividual identification data obtained during bothsystematic and directed surveys

Empirical lagged identification rate data were com-pared to a series of movement models representingclosed and open populations implemented in the pro-gram SOCPROG 29 (Whitehead 2009) (Table 1a)These models provide an estimate of the number ofvisitors in the study area based on markminus recaptureprobabilities (Whitehead 2001) SOCPROG includes 2closed population models but only one of those mod-els (A) was applied because SNE appeared to be anopen population as the discovery curve indicatedthat new right whales were identified in the studyarea over time and the 2 models provided similarresults to this dataset The following pairs of openmodels are structurally identical but parameterizeddifferently B and D C and F and E and G (Table 1)This order represents the order in which the programgenerates the results when the models are run simul-taneously All models were run simultaneously sothat the variance inflation factor could be taken fromthe most general model and applied to all of them(Whitehead 2009) Model selection was based on thelowest Akaikersquos information criterion (AIC) when thedata were overdispersed (Whitehead 2007) other-wise the lowest quasi-AIC (QAIC) was used andmodel fits were bootstrapped 100 times to generateSEs for the lagged identification rate estimates

The lagged identification rate was calculated fromthe best-fit model applied to sighting data collectedfrom December to May the period when previous

255

Endang Species Res 45 251ndash268 2021

studies identified a high right whale presence in thearea (Kraus et al 2016b Leiter et al 2017) Residencywas estimated for the 2 time periods (2011minus2015 and2017minus2018) to determine if it changed over time Thelagged identification rates were calculated andmodels fitted for males and females separately toinvestigate whether the sexes exhibited differentresidency patterns The number of right whale iden-tifications for summer and fall was too low to calcu-late a separate lagged identification rate but the per-centages of individual right whales sighted in thesummer and fall were calculated These models havebeen used for cetaceans (eg Wimmer amp Whitehead2004 Dinis et al 2016 Chabanne et al 2017) andother migratory marine megafauna (eg manta raysDeakos et al 2011 whale sharks McKinney et al2017 McCoy et al 2018)

224 Movements

Dataset 3 was used to estimate the seasonal transi-tion probabilities between SNE and other areas forboth study periods The analysis was limited to themovements between SNE and no more than 4 areas

to ensure precise estimates given by the small num-ber of habitat comparisons and the high number ofidentified individuals moving among areas (White-head 2009) The areas followed Brillant et al (2015)and included from north to south the Gulf of StLawrence Bay of Fundy Gulf of Maine (includingthe Columbia and Jeffreys ledges and Jordan Basin)Cape Cod Bay Great South ChannelminusGeorges Bankand the South (from New York to Florida) (Fig 1B)The mid-Atlantic was combined with adjacent areasto the south to increase the sample size

Transition probabilities were calculated using apara meterized Markov movement model inSOCPROG 29 (Whitehead 2009) This population-scale behavior model uses the locations and eachtime unit of photographically identified individuals toestimate the probability of moving from one area toanother at a time lag (Whitehead 2001) This modelcan be used with identifications that are not distrib-uted randomly or uniformly in space or time and thathave no independent measure of effort (Whitehead2001) The small number (n lt 10) of seasonal rightwhale identifications in SNE in fall and summer2011minus 2015 did not permit the estimation of transitionprobabilities for those seasons A 30 d lag was used

256

aModel Model type and parameters

A Closed (1a1 = N or number of visitors)

B Emigrationmortality (a1 = emigration rate 1a2 = N)

C Emigration + reimmigration (a1 = emigration rate a2(a2 + a3) = proportion of population in study area atany time)

D Emigrationmortality (a1 = N a2 = mean residence time)

E Emigration + reimmigration + mortality

F Emigration + reimmigration (a1 = N a2 = mean time in study area a3 = mean time out of study area)

G Emigration + reimmigration + mortality (a1 = N a2 = mean time in study area a3 = mean time out of studyarea a4 = mortality rate)

bModel All Female Male AIC QAIC AIC QAIC AIC QAIC 2011minus2015 2017minus2018 2011minus2015 2017minus2018 2011minus2015 2017minus2018

A 35732 149084 15468 50423 35750 49668B 35630 147694 15447 50488 89158 48730C 36039 145885a 15674 49626a 35694a 47989a

D 35630 147694 15447 50489 35806 48730E 35979 146659 15770 49796 35906 48663F 35120a 145885a 15340a 49626a 35694a 47989a

G 35289 146084 52378 50268 35872 48291

aBest-fit model (with lowest AIC or QAIC value)

Table 1 (a) Models and parameters and (b) fits and comparison for lagged identification rate of all right whales females and males in southern New England during 2 time periods AIC Akaikersquos information criterion QAIC quasi-AIC

Quintana-Rizzo et al Right whale wind energy areas

based on the assumption that an identified rightwhale in any location could reach any of these otherhabitats within this interval (Brillant et al 2015Davies et al 2015) during the season of interestBack-and-forth movements of right whales betweensouthern New England and nearby areas wereexplored by examining the sighting histories of indi-vidual right whales

3 RESULTS

31 Field effort right whale identificationsand behavioral activities

The combined survey effort in southern New Eng-land covered 111 440 km between March 2011 andDecember 2019 (Table 2) The annual tally of rightwhales reported (not unique whale identifications)from all sightings varied between 28 and 418 (144 plusmn49 whales) A total of 327 unique right whales wereidentified with a mean number of 9 identificationsper survey day At least 16 of these whales were con-firmed dead according to NARWC as of the begin-ning of December 2020 The discovery curve showedan increasing trend in the number of new individualssighted with no clear plateau signal (Fig 2) and bythe end of 2019 87 of the current population hadbeen sighted in SNE throughout the study periodThe discovery curve had a steep slope during the2011minus 2015 surveys and was even steeper in 2017minus2018 suggesting an open population or that sight-ings in the area were underestimated Feeding wasrecorded on more occasions (n = 190 occasions) thansocializing (n = 59 occasions) Feeding was observedin all seasons and years whereas social behaviorswere observed mainly in the winter and spring andwere not observed in 2011 and 2017

32 Datasets and statistical analysis

321 Distribution

Sighting rates varied through time suggesting thatright whales have become more common in recentyears and that their presence now extends beyondthe DecemberminusMay period in SNE No right whaleswere reported in 2011 in Dataset 1 but the NEAqsurveys did not start until October that year Sightingrates varied in most other years (Fig 3 Kruskal-Wallis test = 2067 df = 6 p = 0002) Pairwise com-parisons showed that the sighting rates of right

whales were not significantly different among theearly years of the study and the sighting rates ofmost of those years were lower than those of recentyears (Fig 3) Sighting rates were not statistically dif-ferent in 2015 2017 and 2018 (Fig 3) Right whalesightings by month were highest from January toApril during the early years of the study but inrecent years right whales were sighted in mostmonths of the year with notably high sighting ratesin December 2018 and August 2019 (Fig 4)

The seasonal clustered distribution of right whalesvaried in space and time and extended into wind

257

Year Tally of Unique of NEAq NEFSC CCS right ID population (km) (km) (km) whales plusmn SE

2011 83 53 11 plusmn 1 4279 2455 3272012 28 22 5 plusmn 1 16 042 1471 minus2013 32 20 4 plusmn 1 12 890 779 minus2014 44 43 9 plusmn 1 17 279 1763 minus2015 86 53 11 plusmn 1 9594 6761 3572017 214 122 29 plusmn 2 18 867 2456 minus2018 418 202 53 plusmn 2 11 295 9732 minus2019 250 NA NC 20729 NA minus

Table 2 Total tally of right whales recorded in all sightings(no ID included) unique ID population percentage sightedin relation to the general right whale population (based onPace et al 2017 and Pettis et al 2021 updated population es-timates) and annual survey effort (km) in southern NewEngland waters by main data contributors NEAq NewEngland Aquarium NEFSC Northeast Fisheries ScienceCenter CCS Center for Coastal Studies NA not availableat the time of the data request NC not calculated (number

of unique IDs not available) (ndash) no data

Fig 2 Discovery curve for the number of uniquely identifiedindividual right whales sighted in southern New EnglandThe slope of the curve indicates an open population wherenot all individuals have been sampled No field effort was

conducted in 2016

Endang Species Res 45 251ndash268 2021258

A Mann-Whitney U-test statistical values Year 2012 2013 2014 2015 2017 2018 2019 2012 4950 5600 1600 2650 1800 750 2013 096 5600 1500 2750 1900 1050 2014 075 075 2200 4100 3000 1000 2015 021 017 034 2700 1800 900 2017 004 004 010 095 4300 1850 2018 001 001 004 039 039 2400 2019 0002 0006 0002 011 003 015

p-v

alue

s

2011

Sig

htin

g ra

teno

of r

ight

wha

les

per

100

0 km

of s

urve

y

40

30

20

10

02012 2013 2014 2015 2016 2017 2018 2019

B

Fig 3 (A) Mann-Whitney U-test comparisons and (B) central tendency and variability of sighting rates of right whales Noright whale sightings were reported in 2011 and no field effort was conducted in 2016 in Dataset 1 (sightings and survey effortcollected during aerial surveys conducted by the New England Aquarium) The solid line drawn across each box representsthe median sighting rate of that year The lower boundary is the 25th percentile and the upper boundary is the 75th percentileof a box Lines on the top and bottom of each box represent the largest and smallest frequency sighting rates respectively

excluding outliers (o) and extreme values (Δ) p lt 005

Fig 4 Monthly sighting rates of right whales and monthlyaerial surveys conducted in the study area in Dataset 1(sightings and survey effort collected during aerial surveysconducted by the New England Aquarium) Sighting rate isdefined as the number of right whales per 1000 km of surveyThe number of IDs including resightings is included forthose months in which IDs were available in Dataset 2 (IDscollected by all survey teams) The 2019 IDs were not avail-

able at the time of the data request

Quintana-Rizzo et al Right whale wind energy areas

energy lease sites In the 2011minus2015 winters rightwhale sightings increased in the study area and weremore concentrated in the northeastern wind energyareas and the southern portion of Nantucket Shoals(Fig 5A) However in the 2017minus2019 winters thesightings spanned to the southeastern portion of theshoals (Fig 5B) In the spring right whale distribu-tion shifted to the west in both study periodsalthough in the early years their distribution was fur-ther south of Nantucket (Fig 5CD) Summer sight-ings were only recorded during the 2017minus2019period with right whales sighted in nearshore watersoff Nantucket and along Nantucket Shoals (Fig 5E)

322 Demographics

The ratio of adults to juveniles in SNE was the sameas in the population as a whole during the studyAdult whales were observed significantly more thanjuveniles with an annual mean of 70 adults and30 juveniles The adultjuvenile ratio was signifi-cantly different from year to year (G = 2061 χ2 df = 6p lt 0002) but the annual ratios were not significantlydifferent from the yearly population age ratios(Table 3) indicating that the age ratio of the whalesvisiting the study area followed the age ratio of thepopulation Sex was confirmed for 93 of the identifi-

259

Fig 5 Hotspot analysis of right whale seasonal distribution in the study area (AC 2011ndash2015 BDE 2017ndash2019) with hotspotsbased on significantly higher values than surrounding areas No coldspots were identified Wind energy area lease zones are

identified by numbers Additional details of the study area are shown in Fig 1

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Quintana-Rizzo et al Right whale wind energy areas

cant spatial clustering of right whales by seasons inthe early and recent years of the study using theQGIS Hotspot Analysis plugin (Oxoli et al 2017) Thisplugin implements the Getis-Ord Gi statistic to de-tect atypical clusters of high (hotspots) or low (cold -spots) values by looking at a cell value in the contextof its neighborsrsquo values (Getis amp Ord 1992 Oxoli et al2017) Seasons were defined as winter (DecemberminusFebruary) spring (MarchminusMay) summer (JuneminusAugust) and fall (Septemberminus November) Only sea-sonminusperiod combinations with greater than 10 rightwhale sightings were used as smaller sample sizesare considered insufficient for statistical analysis (Ott1994) Seasonal maps were compiled for each studyperiod at 3 levels of confidence (99 95 and 90)and all clusters that were within the 90 confidencelevel were considered hotspots

222 Demographics

NARWC (2020) provided sex and age class (calfjuvenile adult unknown) information for the indi-vidual right whales sighted in the study area (Dataset2) Only juvenile (defined as whales that are 1minus8 yrold) and adult (defined as whales that are 9 yr of ageor older were not seen as calves but initial sightingwas at least 8 yr prior or were known to be reproduc-tive Hamilton et al 1995) age classes were exam-ined Unknowns and dependent calves were ex -cluded because the number of sightings was toosmall (n lt 10) for statistical comparisons A G-test ofindependence was used to determine if the sex andage ratios differed from year to year and the annualage and sex ratios were compared to the correspon-ding annual ratios of the population using individualG-tests of goodness of fit with a Bonferroni correction(after Mayo et al 2018) Population ratios were calcu-lated using the minimum number of right whalespresumed alive in a given year following Knowlton etal (1994)

Since right whales were present in this region atthe time of year when conception is expected for thisspecies (Cole et al 2013) life history characteristicsof the males and females were investigated Pater-nity is determined through molecular analysis (Frasieret al 2007) and for this study genetic analysis ofknown fathers was only available for the first 3 yrBoth the proportion of reproductive females and theproportion of conceptive females compared to allidentified females present in SNE were calculated foreach year Females that had given birth in the yearsprior to or in the year of a recorded sighting were

considered reproductive (Kraus et al 2001) Femaleswere considered conceptive for a year beginning inMarch 2 yr before giving birth (Cole et al 2013) Forinstance a female first sighted with a calf anywherealong the North Atlantic between December 2014and November 2015 would be considered conceptiveduring the period 1 March 2013 through 1 March2014

223 Residence

Residence was defined as the minimum number ofdays that an individual whale was in SNE (Baracho-Neto et al 2012) To determine the residency of rightwhales in the study area maximum likelihood meth-ods were used to determine the lagged identificationrate ie the probability that an individual rightwhale will be resighted in the study area after a timelag using Dataset 2 (Whitehead 2001) This methodallows for non-random distribution of sampling effort(Whitehead 2007 2009) and the incorporation ofindividual identification data obtained during bothsystematic and directed surveys

Empirical lagged identification rate data were com-pared to a series of movement models representingclosed and open populations implemented in the pro-gram SOCPROG 29 (Whitehead 2009) (Table 1a)These models provide an estimate of the number ofvisitors in the study area based on markminus recaptureprobabilities (Whitehead 2001) SOCPROG includes 2closed population models but only one of those mod-els (A) was applied because SNE appeared to be anopen population as the discovery curve indicatedthat new right whales were identified in the studyarea over time and the 2 models provided similarresults to this dataset The following pairs of openmodels are structurally identical but parameterizeddifferently B and D C and F and E and G (Table 1)This order represents the order in which the programgenerates the results when the models are run simul-taneously All models were run simultaneously sothat the variance inflation factor could be taken fromthe most general model and applied to all of them(Whitehead 2009) Model selection was based on thelowest Akaikersquos information criterion (AIC) when thedata were overdispersed (Whitehead 2007) other-wise the lowest quasi-AIC (QAIC) was used andmodel fits were bootstrapped 100 times to generateSEs for the lagged identification rate estimates

The lagged identification rate was calculated fromthe best-fit model applied to sighting data collectedfrom December to May the period when previous

255

Endang Species Res 45 251ndash268 2021

studies identified a high right whale presence in thearea (Kraus et al 2016b Leiter et al 2017) Residencywas estimated for the 2 time periods (2011minus2015 and2017minus2018) to determine if it changed over time Thelagged identification rates were calculated andmodels fitted for males and females separately toinvestigate whether the sexes exhibited differentresidency patterns The number of right whale iden-tifications for summer and fall was too low to calcu-late a separate lagged identification rate but the per-centages of individual right whales sighted in thesummer and fall were calculated These models havebeen used for cetaceans (eg Wimmer amp Whitehead2004 Dinis et al 2016 Chabanne et al 2017) andother migratory marine megafauna (eg manta raysDeakos et al 2011 whale sharks McKinney et al2017 McCoy et al 2018)

224 Movements

Dataset 3 was used to estimate the seasonal transi-tion probabilities between SNE and other areas forboth study periods The analysis was limited to themovements between SNE and no more than 4 areas

to ensure precise estimates given by the small num-ber of habitat comparisons and the high number ofidentified individuals moving among areas (White-head 2009) The areas followed Brillant et al (2015)and included from north to south the Gulf of StLawrence Bay of Fundy Gulf of Maine (includingthe Columbia and Jeffreys ledges and Jordan Basin)Cape Cod Bay Great South ChannelminusGeorges Bankand the South (from New York to Florida) (Fig 1B)The mid-Atlantic was combined with adjacent areasto the south to increase the sample size

Transition probabilities were calculated using apara meterized Markov movement model inSOCPROG 29 (Whitehead 2009) This population-scale behavior model uses the locations and eachtime unit of photographically identified individuals toestimate the probability of moving from one area toanother at a time lag (Whitehead 2001) This modelcan be used with identifications that are not distrib-uted randomly or uniformly in space or time and thathave no independent measure of effort (Whitehead2001) The small number (n lt 10) of seasonal rightwhale identifications in SNE in fall and summer2011minus 2015 did not permit the estimation of transitionprobabilities for those seasons A 30 d lag was used

256

aModel Model type and parameters

A Closed (1a1 = N or number of visitors)

B Emigrationmortality (a1 = emigration rate 1a2 = N)

C Emigration + reimmigration (a1 = emigration rate a2(a2 + a3) = proportion of population in study area atany time)

D Emigrationmortality (a1 = N a2 = mean residence time)

E Emigration + reimmigration + mortality

F Emigration + reimmigration (a1 = N a2 = mean time in study area a3 = mean time out of study area)

G Emigration + reimmigration + mortality (a1 = N a2 = mean time in study area a3 = mean time out of studyarea a4 = mortality rate)

bModel All Female Male AIC QAIC AIC QAIC AIC QAIC 2011minus2015 2017minus2018 2011minus2015 2017minus2018 2011minus2015 2017minus2018

A 35732 149084 15468 50423 35750 49668B 35630 147694 15447 50488 89158 48730C 36039 145885a 15674 49626a 35694a 47989a

D 35630 147694 15447 50489 35806 48730E 35979 146659 15770 49796 35906 48663F 35120a 145885a 15340a 49626a 35694a 47989a

G 35289 146084 52378 50268 35872 48291

aBest-fit model (with lowest AIC or QAIC value)

Table 1 (a) Models and parameters and (b) fits and comparison for lagged identification rate of all right whales females and males in southern New England during 2 time periods AIC Akaikersquos information criterion QAIC quasi-AIC

Quintana-Rizzo et al Right whale wind energy areas

based on the assumption that an identified rightwhale in any location could reach any of these otherhabitats within this interval (Brillant et al 2015Davies et al 2015) during the season of interestBack-and-forth movements of right whales betweensouthern New England and nearby areas wereexplored by examining the sighting histories of indi-vidual right whales

3 RESULTS

31 Field effort right whale identificationsand behavioral activities

The combined survey effort in southern New Eng-land covered 111 440 km between March 2011 andDecember 2019 (Table 2) The annual tally of rightwhales reported (not unique whale identifications)from all sightings varied between 28 and 418 (144 plusmn49 whales) A total of 327 unique right whales wereidentified with a mean number of 9 identificationsper survey day At least 16 of these whales were con-firmed dead according to NARWC as of the begin-ning of December 2020 The discovery curve showedan increasing trend in the number of new individualssighted with no clear plateau signal (Fig 2) and bythe end of 2019 87 of the current population hadbeen sighted in SNE throughout the study periodThe discovery curve had a steep slope during the2011minus 2015 surveys and was even steeper in 2017minus2018 suggesting an open population or that sight-ings in the area were underestimated Feeding wasrecorded on more occasions (n = 190 occasions) thansocializing (n = 59 occasions) Feeding was observedin all seasons and years whereas social behaviorswere observed mainly in the winter and spring andwere not observed in 2011 and 2017

32 Datasets and statistical analysis

321 Distribution

Sighting rates varied through time suggesting thatright whales have become more common in recentyears and that their presence now extends beyondthe DecemberminusMay period in SNE No right whaleswere reported in 2011 in Dataset 1 but the NEAqsurveys did not start until October that year Sightingrates varied in most other years (Fig 3 Kruskal-Wallis test = 2067 df = 6 p = 0002) Pairwise com-parisons showed that the sighting rates of right

whales were not significantly different among theearly years of the study and the sighting rates ofmost of those years were lower than those of recentyears (Fig 3) Sighting rates were not statistically dif-ferent in 2015 2017 and 2018 (Fig 3) Right whalesightings by month were highest from January toApril during the early years of the study but inrecent years right whales were sighted in mostmonths of the year with notably high sighting ratesin December 2018 and August 2019 (Fig 4)

The seasonal clustered distribution of right whalesvaried in space and time and extended into wind

257

Year Tally of Unique of NEAq NEFSC CCS right ID population (km) (km) (km) whales plusmn SE

2011 83 53 11 plusmn 1 4279 2455 3272012 28 22 5 plusmn 1 16 042 1471 minus2013 32 20 4 plusmn 1 12 890 779 minus2014 44 43 9 plusmn 1 17 279 1763 minus2015 86 53 11 plusmn 1 9594 6761 3572017 214 122 29 plusmn 2 18 867 2456 minus2018 418 202 53 plusmn 2 11 295 9732 minus2019 250 NA NC 20729 NA minus

Table 2 Total tally of right whales recorded in all sightings(no ID included) unique ID population percentage sightedin relation to the general right whale population (based onPace et al 2017 and Pettis et al 2021 updated population es-timates) and annual survey effort (km) in southern NewEngland waters by main data contributors NEAq NewEngland Aquarium NEFSC Northeast Fisheries ScienceCenter CCS Center for Coastal Studies NA not availableat the time of the data request NC not calculated (number

of unique IDs not available) (ndash) no data

Fig 2 Discovery curve for the number of uniquely identifiedindividual right whales sighted in southern New EnglandThe slope of the curve indicates an open population wherenot all individuals have been sampled No field effort was

conducted in 2016

Endang Species Res 45 251ndash268 2021258

A Mann-Whitney U-test statistical values Year 2012 2013 2014 2015 2017 2018 2019 2012 4950 5600 1600 2650 1800 750 2013 096 5600 1500 2750 1900 1050 2014 075 075 2200 4100 3000 1000 2015 021 017 034 2700 1800 900 2017 004 004 010 095 4300 1850 2018 001 001 004 039 039 2400 2019 0002 0006 0002 011 003 015

p-v

alue

s

2011

Sig

htin

g ra

teno

of r

ight

wha

les

per

100

0 km

of s

urve

y

40

30

20

10

02012 2013 2014 2015 2016 2017 2018 2019

B

Fig 3 (A) Mann-Whitney U-test comparisons and (B) central tendency and variability of sighting rates of right whales Noright whale sightings were reported in 2011 and no field effort was conducted in 2016 in Dataset 1 (sightings and survey effortcollected during aerial surveys conducted by the New England Aquarium) The solid line drawn across each box representsthe median sighting rate of that year The lower boundary is the 25th percentile and the upper boundary is the 75th percentileof a box Lines on the top and bottom of each box represent the largest and smallest frequency sighting rates respectively

excluding outliers (o) and extreme values (Δ) p lt 005

Fig 4 Monthly sighting rates of right whales and monthlyaerial surveys conducted in the study area in Dataset 1(sightings and survey effort collected during aerial surveysconducted by the New England Aquarium) Sighting rate isdefined as the number of right whales per 1000 km of surveyThe number of IDs including resightings is included forthose months in which IDs were available in Dataset 2 (IDscollected by all survey teams) The 2019 IDs were not avail-

able at the time of the data request

Quintana-Rizzo et al Right whale wind energy areas

energy lease sites In the 2011minus2015 winters rightwhale sightings increased in the study area and weremore concentrated in the northeastern wind energyareas and the southern portion of Nantucket Shoals(Fig 5A) However in the 2017minus2019 winters thesightings spanned to the southeastern portion of theshoals (Fig 5B) In the spring right whale distribu-tion shifted to the west in both study periodsalthough in the early years their distribution was fur-ther south of Nantucket (Fig 5CD) Summer sight-ings were only recorded during the 2017minus2019period with right whales sighted in nearshore watersoff Nantucket and along Nantucket Shoals (Fig 5E)

322 Demographics

The ratio of adults to juveniles in SNE was the sameas in the population as a whole during the studyAdult whales were observed significantly more thanjuveniles with an annual mean of 70 adults and30 juveniles The adultjuvenile ratio was signifi-cantly different from year to year (G = 2061 χ2 df = 6p lt 0002) but the annual ratios were not significantlydifferent from the yearly population age ratios(Table 3) indicating that the age ratio of the whalesvisiting the study area followed the age ratio of thepopulation Sex was confirmed for 93 of the identifi-

259

Fig 5 Hotspot analysis of right whale seasonal distribution in the study area (AC 2011ndash2015 BDE 2017ndash2019) with hotspotsbased on significantly higher values than surrounding areas No coldspots were identified Wind energy area lease zones are

identified by numbers Additional details of the study area are shown in Fig 1

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Endang Species Res 45 251ndash268 2021

studies identified a high right whale presence in thearea (Kraus et al 2016b Leiter et al 2017) Residencywas estimated for the 2 time periods (2011minus2015 and2017minus2018) to determine if it changed over time Thelagged identification rates were calculated andmodels fitted for males and females separately toinvestigate whether the sexes exhibited differentresidency patterns The number of right whale iden-tifications for summer and fall was too low to calcu-late a separate lagged identification rate but the per-centages of individual right whales sighted in thesummer and fall were calculated These models havebeen used for cetaceans (eg Wimmer amp Whitehead2004 Dinis et al 2016 Chabanne et al 2017) andother migratory marine megafauna (eg manta raysDeakos et al 2011 whale sharks McKinney et al2017 McCoy et al 2018)

224 Movements

Dataset 3 was used to estimate the seasonal transi-tion probabilities between SNE and other areas forboth study periods The analysis was limited to themovements between SNE and no more than 4 areas

to ensure precise estimates given by the small num-ber of habitat comparisons and the high number ofidentified individuals moving among areas (White-head 2009) The areas followed Brillant et al (2015)and included from north to south the Gulf of StLawrence Bay of Fundy Gulf of Maine (includingthe Columbia and Jeffreys ledges and Jordan Basin)Cape Cod Bay Great South ChannelminusGeorges Bankand the South (from New York to Florida) (Fig 1B)The mid-Atlantic was combined with adjacent areasto the south to increase the sample size

Transition probabilities were calculated using apara meterized Markov movement model inSOCPROG 29 (Whitehead 2009) This population-scale behavior model uses the locations and eachtime unit of photographically identified individuals toestimate the probability of moving from one area toanother at a time lag (Whitehead 2001) This modelcan be used with identifications that are not distrib-uted randomly or uniformly in space or time and thathave no independent measure of effort (Whitehead2001) The small number (n lt 10) of seasonal rightwhale identifications in SNE in fall and summer2011minus 2015 did not permit the estimation of transitionprobabilities for those seasons A 30 d lag was used

256

aModel Model type and parameters

A Closed (1a1 = N or number of visitors)

B Emigrationmortality (a1 = emigration rate 1a2 = N)

C Emigration + reimmigration (a1 = emigration rate a2(a2 + a3) = proportion of population in study area atany time)

D Emigrationmortality (a1 = N a2 = mean residence time)

E Emigration + reimmigration + mortality

F Emigration + reimmigration (a1 = N a2 = mean time in study area a3 = mean time out of study area)

G Emigration + reimmigration + mortality (a1 = N a2 = mean time in study area a3 = mean time out of studyarea a4 = mortality rate)

bModel All Female Male AIC QAIC AIC QAIC AIC QAIC 2011minus2015 2017minus2018 2011minus2015 2017minus2018 2011minus2015 2017minus2018

A 35732 149084 15468 50423 35750 49668B 35630 147694 15447 50488 89158 48730C 36039 145885a 15674 49626a 35694a 47989a

D 35630 147694 15447 50489 35806 48730E 35979 146659 15770 49796 35906 48663F 35120a 145885a 15340a 49626a 35694a 47989a

G 35289 146084 52378 50268 35872 48291

aBest-fit model (with lowest AIC or QAIC value)

Table 1 (a) Models and parameters and (b) fits and comparison for lagged identification rate of all right whales females and males in southern New England during 2 time periods AIC Akaikersquos information criterion QAIC quasi-AIC

Quintana-Rizzo et al Right whale wind energy areas

based on the assumption that an identified rightwhale in any location could reach any of these otherhabitats within this interval (Brillant et al 2015Davies et al 2015) during the season of interestBack-and-forth movements of right whales betweensouthern New England and nearby areas wereexplored by examining the sighting histories of indi-vidual right whales

3 RESULTS

31 Field effort right whale identificationsand behavioral activities

The combined survey effort in southern New Eng-land covered 111 440 km between March 2011 andDecember 2019 (Table 2) The annual tally of rightwhales reported (not unique whale identifications)from all sightings varied between 28 and 418 (144 plusmn49 whales) A total of 327 unique right whales wereidentified with a mean number of 9 identificationsper survey day At least 16 of these whales were con-firmed dead according to NARWC as of the begin-ning of December 2020 The discovery curve showedan increasing trend in the number of new individualssighted with no clear plateau signal (Fig 2) and bythe end of 2019 87 of the current population hadbeen sighted in SNE throughout the study periodThe discovery curve had a steep slope during the2011minus 2015 surveys and was even steeper in 2017minus2018 suggesting an open population or that sight-ings in the area were underestimated Feeding wasrecorded on more occasions (n = 190 occasions) thansocializing (n = 59 occasions) Feeding was observedin all seasons and years whereas social behaviorswere observed mainly in the winter and spring andwere not observed in 2011 and 2017

32 Datasets and statistical analysis

321 Distribution

Sighting rates varied through time suggesting thatright whales have become more common in recentyears and that their presence now extends beyondthe DecemberminusMay period in SNE No right whaleswere reported in 2011 in Dataset 1 but the NEAqsurveys did not start until October that year Sightingrates varied in most other years (Fig 3 Kruskal-Wallis test = 2067 df = 6 p = 0002) Pairwise com-parisons showed that the sighting rates of right

whales were not significantly different among theearly years of the study and the sighting rates ofmost of those years were lower than those of recentyears (Fig 3) Sighting rates were not statistically dif-ferent in 2015 2017 and 2018 (Fig 3) Right whalesightings by month were highest from January toApril during the early years of the study but inrecent years right whales were sighted in mostmonths of the year with notably high sighting ratesin December 2018 and August 2019 (Fig 4)

The seasonal clustered distribution of right whalesvaried in space and time and extended into wind

257

Year Tally of Unique of NEAq NEFSC CCS right ID population (km) (km) (km) whales plusmn SE

2011 83 53 11 plusmn 1 4279 2455 3272012 28 22 5 plusmn 1 16 042 1471 minus2013 32 20 4 plusmn 1 12 890 779 minus2014 44 43 9 plusmn 1 17 279 1763 minus2015 86 53 11 plusmn 1 9594 6761 3572017 214 122 29 plusmn 2 18 867 2456 minus2018 418 202 53 plusmn 2 11 295 9732 minus2019 250 NA NC 20729 NA minus

Table 2 Total tally of right whales recorded in all sightings(no ID included) unique ID population percentage sightedin relation to the general right whale population (based onPace et al 2017 and Pettis et al 2021 updated population es-timates) and annual survey effort (km) in southern NewEngland waters by main data contributors NEAq NewEngland Aquarium NEFSC Northeast Fisheries ScienceCenter CCS Center for Coastal Studies NA not availableat the time of the data request NC not calculated (number

of unique IDs not available) (ndash) no data

Fig 2 Discovery curve for the number of uniquely identifiedindividual right whales sighted in southern New EnglandThe slope of the curve indicates an open population wherenot all individuals have been sampled No field effort was

conducted in 2016

Endang Species Res 45 251ndash268 2021258

A Mann-Whitney U-test statistical values Year 2012 2013 2014 2015 2017 2018 2019 2012 4950 5600 1600 2650 1800 750 2013 096 5600 1500 2750 1900 1050 2014 075 075 2200 4100 3000 1000 2015 021 017 034 2700 1800 900 2017 004 004 010 095 4300 1850 2018 001 001 004 039 039 2400 2019 0002 0006 0002 011 003 015

p-v

alue

s

2011

Sig

htin

g ra

teno

of r

ight

wha

les

per

100

0 km

of s

urve

y

40

30

20

10

02012 2013 2014 2015 2016 2017 2018 2019

B

Fig 3 (A) Mann-Whitney U-test comparisons and (B) central tendency and variability of sighting rates of right whales Noright whale sightings were reported in 2011 and no field effort was conducted in 2016 in Dataset 1 (sightings and survey effortcollected during aerial surveys conducted by the New England Aquarium) The solid line drawn across each box representsthe median sighting rate of that year The lower boundary is the 25th percentile and the upper boundary is the 75th percentileof a box Lines on the top and bottom of each box represent the largest and smallest frequency sighting rates respectively

excluding outliers (o) and extreme values (Δ) p lt 005

Fig 4 Monthly sighting rates of right whales and monthlyaerial surveys conducted in the study area in Dataset 1(sightings and survey effort collected during aerial surveysconducted by the New England Aquarium) Sighting rate isdefined as the number of right whales per 1000 km of surveyThe number of IDs including resightings is included forthose months in which IDs were available in Dataset 2 (IDscollected by all survey teams) The 2019 IDs were not avail-

able at the time of the data request

Quintana-Rizzo et al Right whale wind energy areas

energy lease sites In the 2011minus2015 winters rightwhale sightings increased in the study area and weremore concentrated in the northeastern wind energyareas and the southern portion of Nantucket Shoals(Fig 5A) However in the 2017minus2019 winters thesightings spanned to the southeastern portion of theshoals (Fig 5B) In the spring right whale distribu-tion shifted to the west in both study periodsalthough in the early years their distribution was fur-ther south of Nantucket (Fig 5CD) Summer sight-ings were only recorded during the 2017minus2019period with right whales sighted in nearshore watersoff Nantucket and along Nantucket Shoals (Fig 5E)

322 Demographics

The ratio of adults to juveniles in SNE was the sameas in the population as a whole during the studyAdult whales were observed significantly more thanjuveniles with an annual mean of 70 adults and30 juveniles The adultjuvenile ratio was signifi-cantly different from year to year (G = 2061 χ2 df = 6p lt 0002) but the annual ratios were not significantlydifferent from the yearly population age ratios(Table 3) indicating that the age ratio of the whalesvisiting the study area followed the age ratio of thepopulation Sex was confirmed for 93 of the identifi-

259

Fig 5 Hotspot analysis of right whale seasonal distribution in the study area (AC 2011ndash2015 BDE 2017ndash2019) with hotspotsbased on significantly higher values than surrounding areas No coldspots were identified Wind energy area lease zones are

identified by numbers Additional details of the study area are shown in Fig 1

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

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Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Quintana-Rizzo et al Right whale wind energy areas

based on the assumption that an identified rightwhale in any location could reach any of these otherhabitats within this interval (Brillant et al 2015Davies et al 2015) during the season of interestBack-and-forth movements of right whales betweensouthern New England and nearby areas wereexplored by examining the sighting histories of indi-vidual right whales

3 RESULTS

31 Field effort right whale identificationsand behavioral activities

The combined survey effort in southern New Eng-land covered 111 440 km between March 2011 andDecember 2019 (Table 2) The annual tally of rightwhales reported (not unique whale identifications)from all sightings varied between 28 and 418 (144 plusmn49 whales) A total of 327 unique right whales wereidentified with a mean number of 9 identificationsper survey day At least 16 of these whales were con-firmed dead according to NARWC as of the begin-ning of December 2020 The discovery curve showedan increasing trend in the number of new individualssighted with no clear plateau signal (Fig 2) and bythe end of 2019 87 of the current population hadbeen sighted in SNE throughout the study periodThe discovery curve had a steep slope during the2011minus 2015 surveys and was even steeper in 2017minus2018 suggesting an open population or that sight-ings in the area were underestimated Feeding wasrecorded on more occasions (n = 190 occasions) thansocializing (n = 59 occasions) Feeding was observedin all seasons and years whereas social behaviorswere observed mainly in the winter and spring andwere not observed in 2011 and 2017

32 Datasets and statistical analysis

321 Distribution

Sighting rates varied through time suggesting thatright whales have become more common in recentyears and that their presence now extends beyondthe DecemberminusMay period in SNE No right whaleswere reported in 2011 in Dataset 1 but the NEAqsurveys did not start until October that year Sightingrates varied in most other years (Fig 3 Kruskal-Wallis test = 2067 df = 6 p = 0002) Pairwise com-parisons showed that the sighting rates of right

whales were not significantly different among theearly years of the study and the sighting rates ofmost of those years were lower than those of recentyears (Fig 3) Sighting rates were not statistically dif-ferent in 2015 2017 and 2018 (Fig 3) Right whalesightings by month were highest from January toApril during the early years of the study but inrecent years right whales were sighted in mostmonths of the year with notably high sighting ratesin December 2018 and August 2019 (Fig 4)

The seasonal clustered distribution of right whalesvaried in space and time and extended into wind

257

Year Tally of Unique of NEAq NEFSC CCS right ID population (km) (km) (km) whales plusmn SE

2011 83 53 11 plusmn 1 4279 2455 3272012 28 22 5 plusmn 1 16 042 1471 minus2013 32 20 4 plusmn 1 12 890 779 minus2014 44 43 9 plusmn 1 17 279 1763 minus2015 86 53 11 plusmn 1 9594 6761 3572017 214 122 29 plusmn 2 18 867 2456 minus2018 418 202 53 plusmn 2 11 295 9732 minus2019 250 NA NC 20729 NA minus

Table 2 Total tally of right whales recorded in all sightings(no ID included) unique ID population percentage sightedin relation to the general right whale population (based onPace et al 2017 and Pettis et al 2021 updated population es-timates) and annual survey effort (km) in southern NewEngland waters by main data contributors NEAq NewEngland Aquarium NEFSC Northeast Fisheries ScienceCenter CCS Center for Coastal Studies NA not availableat the time of the data request NC not calculated (number

of unique IDs not available) (ndash) no data

Fig 2 Discovery curve for the number of uniquely identifiedindividual right whales sighted in southern New EnglandThe slope of the curve indicates an open population wherenot all individuals have been sampled No field effort was

conducted in 2016

Endang Species Res 45 251ndash268 2021258

A Mann-Whitney U-test statistical values Year 2012 2013 2014 2015 2017 2018 2019 2012 4950 5600 1600 2650 1800 750 2013 096 5600 1500 2750 1900 1050 2014 075 075 2200 4100 3000 1000 2015 021 017 034 2700 1800 900 2017 004 004 010 095 4300 1850 2018 001 001 004 039 039 2400 2019 0002 0006 0002 011 003 015

p-v

alue

s

2011

Sig

htin

g ra

teno

of r

ight

wha

les

per

100

0 km

of s

urve

y

40

30

20

10

02012 2013 2014 2015 2016 2017 2018 2019

B

Fig 3 (A) Mann-Whitney U-test comparisons and (B) central tendency and variability of sighting rates of right whales Noright whale sightings were reported in 2011 and no field effort was conducted in 2016 in Dataset 1 (sightings and survey effortcollected during aerial surveys conducted by the New England Aquarium) The solid line drawn across each box representsthe median sighting rate of that year The lower boundary is the 25th percentile and the upper boundary is the 75th percentileof a box Lines on the top and bottom of each box represent the largest and smallest frequency sighting rates respectively

excluding outliers (o) and extreme values (Δ) p lt 005

Fig 4 Monthly sighting rates of right whales and monthlyaerial surveys conducted in the study area in Dataset 1(sightings and survey effort collected during aerial surveysconducted by the New England Aquarium) Sighting rate isdefined as the number of right whales per 1000 km of surveyThe number of IDs including resightings is included forthose months in which IDs were available in Dataset 2 (IDscollected by all survey teams) The 2019 IDs were not avail-

able at the time of the data request

Quintana-Rizzo et al Right whale wind energy areas

energy lease sites In the 2011minus2015 winters rightwhale sightings increased in the study area and weremore concentrated in the northeastern wind energyareas and the southern portion of Nantucket Shoals(Fig 5A) However in the 2017minus2019 winters thesightings spanned to the southeastern portion of theshoals (Fig 5B) In the spring right whale distribu-tion shifted to the west in both study periodsalthough in the early years their distribution was fur-ther south of Nantucket (Fig 5CD) Summer sight-ings were only recorded during the 2017minus2019period with right whales sighted in nearshore watersoff Nantucket and along Nantucket Shoals (Fig 5E)

322 Demographics

The ratio of adults to juveniles in SNE was the sameas in the population as a whole during the studyAdult whales were observed significantly more thanjuveniles with an annual mean of 70 adults and30 juveniles The adultjuvenile ratio was signifi-cantly different from year to year (G = 2061 χ2 df = 6p lt 0002) but the annual ratios were not significantlydifferent from the yearly population age ratios(Table 3) indicating that the age ratio of the whalesvisiting the study area followed the age ratio of thepopulation Sex was confirmed for 93 of the identifi-

259

Fig 5 Hotspot analysis of right whale seasonal distribution in the study area (AC 2011ndash2015 BDE 2017ndash2019) with hotspotsbased on significantly higher values than surrounding areas No coldspots were identified Wind energy area lease zones are

identified by numbers Additional details of the study area are shown in Fig 1

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Endang Species Res 45 251ndash268 2021258

A Mann-Whitney U-test statistical values Year 2012 2013 2014 2015 2017 2018 2019 2012 4950 5600 1600 2650 1800 750 2013 096 5600 1500 2750 1900 1050 2014 075 075 2200 4100 3000 1000 2015 021 017 034 2700 1800 900 2017 004 004 010 095 4300 1850 2018 001 001 004 039 039 2400 2019 0002 0006 0002 011 003 015

p-v

alue

s

2011

Sig

htin

g ra

teno

of r

ight

wha

les

per

100

0 km

of s

urve

y

40

30

20

10

02012 2013 2014 2015 2016 2017 2018 2019

B

Fig 3 (A) Mann-Whitney U-test comparisons and (B) central tendency and variability of sighting rates of right whales Noright whale sightings were reported in 2011 and no field effort was conducted in 2016 in Dataset 1 (sightings and survey effortcollected during aerial surveys conducted by the New England Aquarium) The solid line drawn across each box representsthe median sighting rate of that year The lower boundary is the 25th percentile and the upper boundary is the 75th percentileof a box Lines on the top and bottom of each box represent the largest and smallest frequency sighting rates respectively

excluding outliers (o) and extreme values (Δ) p lt 005

Fig 4 Monthly sighting rates of right whales and monthlyaerial surveys conducted in the study area in Dataset 1(sightings and survey effort collected during aerial surveysconducted by the New England Aquarium) Sighting rate isdefined as the number of right whales per 1000 km of surveyThe number of IDs including resightings is included forthose months in which IDs were available in Dataset 2 (IDscollected by all survey teams) The 2019 IDs were not avail-

able at the time of the data request

Quintana-Rizzo et al Right whale wind energy areas

energy lease sites In the 2011minus2015 winters rightwhale sightings increased in the study area and weremore concentrated in the northeastern wind energyareas and the southern portion of Nantucket Shoals(Fig 5A) However in the 2017minus2019 winters thesightings spanned to the southeastern portion of theshoals (Fig 5B) In the spring right whale distribu-tion shifted to the west in both study periodsalthough in the early years their distribution was fur-ther south of Nantucket (Fig 5CD) Summer sight-ings were only recorded during the 2017minus2019period with right whales sighted in nearshore watersoff Nantucket and along Nantucket Shoals (Fig 5E)

322 Demographics

The ratio of adults to juveniles in SNE was the sameas in the population as a whole during the studyAdult whales were observed significantly more thanjuveniles with an annual mean of 70 adults and30 juveniles The adultjuvenile ratio was signifi-cantly different from year to year (G = 2061 χ2 df = 6p lt 0002) but the annual ratios were not significantlydifferent from the yearly population age ratios(Table 3) indicating that the age ratio of the whalesvisiting the study area followed the age ratio of thepopulation Sex was confirmed for 93 of the identifi-

259

Fig 5 Hotspot analysis of right whale seasonal distribution in the study area (AC 2011ndash2015 BDE 2017ndash2019) with hotspotsbased on significantly higher values than surrounding areas No coldspots were identified Wind energy area lease zones are

identified by numbers Additional details of the study area are shown in Fig 1

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Quintana-Rizzo et al Right whale wind energy areas

energy lease sites In the 2011minus2015 winters rightwhale sightings increased in the study area and weremore concentrated in the northeastern wind energyareas and the southern portion of Nantucket Shoals(Fig 5A) However in the 2017minus2019 winters thesightings spanned to the southeastern portion of theshoals (Fig 5B) In the spring right whale distribu-tion shifted to the west in both study periodsalthough in the early years their distribution was fur-ther south of Nantucket (Fig 5CD) Summer sight-ings were only recorded during the 2017minus2019period with right whales sighted in nearshore watersoff Nantucket and along Nantucket Shoals (Fig 5E)

322 Demographics

The ratio of adults to juveniles in SNE was the sameas in the population as a whole during the studyAdult whales were observed significantly more thanjuveniles with an annual mean of 70 adults and30 juveniles The adultjuvenile ratio was signifi-cantly different from year to year (G = 2061 χ2 df = 6p lt 0002) but the annual ratios were not significantlydifferent from the yearly population age ratios(Table 3) indicating that the age ratio of the whalesvisiting the study area followed the age ratio of thepopulation Sex was confirmed for 93 of the identifi-

259

Fig 5 Hotspot analysis of right whale seasonal distribution in the study area (AC 2011ndash2015 BDE 2017ndash2019) with hotspotsbased on significantly higher values than surrounding areas No coldspots were identified Wind energy area lease zones are

identified by numbers Additional details of the study area are shown in Fig 1

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Endang Species Res 45 251ndash268 2021

able right whale individuals Of these 181 were malesand 125 were females The sex ratios did not vary sig-nificantly from year to year (G = 204 df = 6 p = 092)The mean annual percentage of malesand females was 57 and 39 respec-tively The observed sex ratio and thepopulation sex ratio did not vary signifi-cantly (Table 3)

Both reproductive females and con-ceptive females were seen in the studyarea Forty-five of the 108 reproduc-tively active females (42) known tobe alive during the study were sightedin SNE and 17 were resighted in mul-tiple years The overall yearly propor-tions of reproductively active femalesvaried from 025 to 057 (041 plusmn 005)In the case of conceptive females only4 females were identified in 4 years(2011 2012 2017 2018) and theiryearly proportion varied from 0 to 014(003 plusmn 002) Except for 1 conceptivefemale which was sighted twice theothers were sighted only once in thestudy area during their conceptionperiod The genetic information ofknown fathers was only available for2011minus2013 Of the 13 known fathersonly 2 were sighted (once) in SNE butnot during the conceptive period

Dependent calf sightings wereuncommon in SNE and only descrip-tive statistics are provided A total of89 right whale calves were born in thepopulation be tween 2011 and 2019but only 6 different calves (inferred by

the presence of known mothers)were recorded during the study inSNE (4 in 2011 1 in 2015 1 in2019) Three calves were sightedtwice in the same year

323 Residence

Individual sighting frequencyover the study period varied be-tween 1 and 10 d suggesting differ-ent degrees of residency (Fig 6)Most right whales (62 n = 202)were sighted more than once overthe course of the study and 42 ofthose whales were sighted in be-

tween 2 and 6 years (2 plusmn 005 years) (Fig 6) Onewhale was sighted nearly every year except in 2013Within a season 147 whales were sighted multiple

260

Year Adult Juvenile SNE vs population Male Female SNE vs population age ratios sex ratios G-test (df) p G-test (df) p

2011 28 20 196 (1) 100 26 24 082 (1) 1002012 11 8 221 (1) 100 12 7 018 (1) 1002013 11 8 245 (1) 100 10 8 006 (1) 1002014 24 18 262 (1) 021 26 17 008 (1) 1002015 30 18 289 (1) 049 29 20 002 (1) 1002017 81 34 364 (1) 028 66 49 004 (1) 1002018 156 38 500 (1) 100 117 72 100 (1) 100

Table 3 Annual numbers of unique adult juvenile male and female right whalessighted in southern New England (SNE) and statistical results of age ratio and sexratio comparisons to the population ratios (NARWC 2020) using a G-test of good-ness of fit with Bonferroni corrected p-values Annual total numbers of whales ofdifferent age and gender classes are not equal because demographic parameters

were not always known for all individuals

A Resightings in days seasons and years

Parameter 2011 2012 2013 2014 2015 2017 2018

Unique IDs 53 22 20 43 53 122 202Resightings in the same season 12 0 0 3 2 43 87Resightings among seasons 0 0 0 0 2 13 44

B Unique IDs and resightings by year

Fig 6 Different resighting patterns of uniquely identified right whales at dif-ferent time scales including (A) during the same season and among seasonsand (B) by year in southern New England between 2011 and 2018 No field

effort was conducted in 2016

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Quintana-Rizzo et al Right whale wind energy areas

times (le5) and 59 whales were sighted several times(le3) in different seasons of the same year Summerand fall sightings were only common in recent yearsand 14 individuals were sighted more than once dur-ing this period Whales resighted the most times in -cluded individuals of both sexes as well as adults andjuveniles although the 3 most sighted animals wereall males (2 adults and 1 juvenile sighted 8minus10 times)

Model F (emigration + reimmigration) was thebest-fit model to describe the residency of the rightwhale population in the study area (Table 1b) fromDecember to May indicating that whales enterleave and reenter the study area during this periodIn the early years the model indicated that on aver-age 54 plusmn 31 whales were in the study area at any onetime during those months and that an individualremained there for an average period of 9 plusmn 7 d(Table 4) However in recent years the number ofwhales estimated to be in the study area duringDecember to May was 65 plusmn 18 right whales and theresidency for both sexes was approximately 13 plusmn 12 d(Table 4) However these results need to be takenwith caution as bootstrap estimates of the SEsaround the estimates were in some cases 15 timesthe mean Model C (emigration + reimmigration) wasalso the best fit to explain the emigration rate andproportion of females and males in the study area(Table 1) This model indicated that the emigrationrate of females is about 5 times higher than that ofmales and that 23 of the population could be pres-ent in the study area from December to May

324 Movements

The transition probabilities of individual whalesvaried throughout the study In the winter and springthe probability of any right whale emigrating from the

study area was 3 times higher in 2011minus2015 than in2017minus2018 (Table 5) In the early winters the Gulf ofMaine and Cape Cod Bay were the top-ranking desti-nations for right whales sighted in SNE withtransition probabilities ranging from 021 to 030(Table 5) In the same period the Gulf of Maine CapeCod Bay and the Great South Channelminus GeorgesBank were the most likely destinations along the UScoast for all emigrating right whales (Table 5) How-ever in recent winters the Great South ChannelminusGeorges Bank (destination probability Pi = 045) andSNE (Pi = 047) ranked high among the most likelydestinations for right whales within the USA In thespring other areas were more visited During the2011minus2015 spring the South (New YorkminusFlorida) wasthe top-ranking destination for right whales emigrat-ing from SNE as well as other regions within theUSA but whales sighted in the SNE region also had ahigh probability of staying in the study area (070) Inthe 2017minus2018 spring the probability of right whalestraveling to the South changed from 069 to 030(Table 5) while Cape Cod Bay (Pi = 055) SNE (Pi =049) and the Gulf of Maine (Pi = 044) ranked highlyas destinations In recent summers SNE and the Gulfof St Lawrence were the high-ranking destinations(Table 5)

Sighting histories of a small percentage of rightwhales (n = 14 lt5) identified in the study areashowed movement back and forth between areasmainly be tween SNE and Cape Cod Bay and betweenSNE and the South (New York) Eleven right whalesin cluding 6 adult males 3 adult females and 2 juve-nile males were first sighted in Cape Cod Bay(ge1 time) then once in SNE and then again in CapeCod Bay (ge1 time) The number of days betweensightings of a whale at these 2 areas ranged from 3 to42 d The other 3 right whales were first sighted inSNE then in either Cape Cod Bay or the South (New

261

Model type and parameters 2011minus2015 2017minus2018 All Female Male All Female Male

F Emigration + reimmigrationNumber of visitors 54 plusmn 31 14 plusmn 7 18 plusmn 33 65 plusmn 18 28 plusmn 13 36 plusmn 9 Time in (d) 9 plusmn 7 4 plusmn 3 5 plusmn 43 13 plusmn 12 15 plusmn 24 18 plusmn 51 Time out (d) 63 plusmn 42 21 plusmn 24 41 plusmn 163 50 plusmn 46 64 plusmn 70 97 plusmn 136

C Emigration + reimmigration Emigration rate ndash ndash 025 plusmn 206 010 plusmn 091 033 plusmn 139 006 plusmn 153 Proportion of population in ndash ndash 009 plusmn 00001 023 plusmn 0001 014 plusmn 00001 017 plusmn 00002

study area at any time

Table 4 Parameters of the model(s) plusmn standard error that best fit the lag identification rates of all right whales including fe-males and males in southern New England DecemberminusMay during the study periods 2011minus2015 and 2017minus2018 Time inout

time spent inoutside of the study area (ndash) not applicable

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Endang Species Res 45 251ndash268 2021

York) and then again in SNE (1 adult male 1 juvenilemale 1 adult female) The gap between sightings ofan individual moving between these areas varied be-tween 19 and 78 d The gap in resighting times is likelymore of a reflection of survey effort than of the whalesrsquomovements among locations

4 DISCUSSION

This 8 yr analysis of sightings re vealed that rightwhales have be come more common in SNE waterswith sightings now documented in nearly everymonth of the year Sighting rates were highest in thespan from winter through early spring and some timeseven during the summer months (eg August 2019)

Our effort included off-transect periods such as cir-cling cross-legs and transits (Leiter et al 2017)Thus sighting rates estimated by this analysis shouldbe compared only to studies using a similar analyticalapproach Close to a quarter of the population may bein this area at any given time between December andMay and the annual percentage of right whales iden-tified varied between 4 and 53 (13 plusmn 4) of theminimum right whale population SNE is also an im-portant habitat used by all demographic groups be-cause the age and sex ratios are similar to those in theoverall species population and the estimated resi-dency duration for females and males tripled duringthe study period The apparent increased use of thishabitat could be related to an increased field effort inrecent years which resulted in a higher number of

262

2011minus2015 2017minus2018 Winter destination Winter destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 080 003 008 004 004 020 CCB lt001 030 016 053 lt001 070 069 004 015 012 031SNE 021 029 033 011 006 067 002 080 018 lt001 020GSB 016 014 011 059 008 049 012 028 061 lt001 040SOU 008 003 0001 001 008 013 013 015 013 060 040Pi 045 050 036 068 017 027 047 045 012

Spring destination Spring destinationOrigin GSLa BOFa GOM CCB SNE GSB SOU Pe GSLb BOFa GOM CCB SNE GSB SOU Pe

GSL BOF GOM 034 014 014 006 032 066 019 044 009 010 017 081CCB 004 082 003 006 004 018 024 073 lt001 002 lt001 027SNE lt001 007 072 008 014 029 lt001 004 089 001 006 011GSB 014 009 005 055 019 047 009 003 017 064 007 036SOU 007 016 016 012 041 051 010 004 023 006 058 042Pi 024 046 039 032 069 044 055 049 019 030

Summer destination Origin GSL BOF GOMb CCBa SNE GSBb SOUa Pe

GSL 088 lt001 012 012 BOF 009 072 019 028 GOM CCB SNE 012 005 082 087 GSB SOU Pi 021 005 031

aNo sightings bSmall sample size thus no probabilities calculated

Table 5 Seasonal transition probabilities of right whales moving between southern New England (SNE) and other right whale areas along theNorth Atlantic Destination probabilities (columns) are shown as Pi and origin probabilities (rows) are shown as Pe including the probability ofstaying within the original region of the sighting (diagonal) There were no data for summer destination 2011ndash2015 GSL Gulf of St LawrenceBOF Bay of Fundy GOM Gulf of Maine CCB Cape Cod Bay GSB Great South ChannelminusGeorges Bank SOU South (New YorkminusFlorida)

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Quintana-Rizzo et al Right whale wind energy areas

identifications andor to dramatic climate-drivenecosystem changes that have oc curred in the pastdecade (Record et al 2019) Migratory species suchas right whales are particularly affected by climatechange because they rely on highly productive sea-sonal habitats (Robinson et al 2009)

Right whales exhibit partial migration (Gowan et al2019) a term used to describe a species in which aproportion of a population stays resident in a habitat(s)and another proportion migrates to another habitat(s)(Chapman et al 2011) It is a widespread phenomenonin invertebrates (Menz et al 2019) fish (Chapman etal 2012) birds (Lundberg 1988) and mammals (Ca-gnacci et al 2011 Martin et al 2018 Berg et al 2019)In the case of right whales all demographic groupshave the potential to migrate to the wintering groundsoff the southeastern USA but the migration appearsto be condition dependent and varies across demo-graphic groups and years Fe males may overwinter inthe feeding areas in the north and skip the breedinggrounds in the south in the years immediately preced-ing and following calving to increase their energystores for future reproduction (Gowan et al 2019) Onthe other hand juveniles and adult males may travelto the southern wintering grounds following years ofhigher prey availability in a northern fall feedingground (Gowan et al 2019)

The mixture of movement patterns within the pop-ulation and the geographical location of SNE sug-gests that the area could be a feeding location forwhales that stay in the mid-Atlantic and north duringthe winterminusspring months and a stopover site forwhales migrating to and from the calving groundsFor example a female right whale initially tagged offthe coast of Virginia in March 2021 traveled for 13 dto SNE where she stayed for 3 d before travelingnorth towards Cape Cod Bay (D Engelhaupt perscomm) Because of the complex movements dis-played by the species our use of the term residencedescribes the minimum time a right whale couldspend in SNE regardless of the overall movementthat the whale exhibited at that time It does not sug-gest that right whales overwinter in SNE

Our findings show that SNE is an important transi-tion region as the whales that utilized the areamoved to and from critical habitats including CapeCod Bay the Gulf of Maine and the Great SouthChannelndash Georges Bank and in the summer manytraveled on to the Gulf of St Lawrence Florida andGeorgia were more frequent destinations when calv-ing rates were higher (Pace et al 2017) in the earlystudy period but the recent low transition rates couldbe due to a lack of births in 2018 or changes in survey

efforts and right whale movements The sightings ofSNE whales in Canadian waters and multiple USAlocations including the mid-Atlantic emphasize theneed for protecting coastal areas that serve as migra-tory corridors

Right whales may utilize SNE as a feeding groundmore often than as a social or mating ground al -though behaviors linked to both activities have beenobserved in the area Feeding was recorded on moreoccasions than socializing and it was observed in allseasons whereas surface active groups were ob -served mainly in the winter and spring Preliminaryresults of oceanographic surveys conducted in watersnear right whale sightings suggest that their diet in-cludes multiple zooplankton species including Cala -nus finmarchius and Centropages sp (Quintana-Rizzo et al 2018) Evidence of feeding throughout theseasons provides support for the extension of USfeeding critical habitats into SNE waters

Almost 50 of reproductive females utilized thisarea within the study period which is an importantconsideration for the speciesrsquo conservation since theoverall population has declined significantly (Pace etal 2017 Corkeron et al 2018) Conceptive femaleswere not often seen and their proportional presencewas not as high as in the inferred mating groundidentified by Cole et al (2013) over a decade agoHowever large numbers of conceptive females arenot required for mating to occur because matinggroups often consist of many males and 1 female(Kraus amp Hatch 2001) Few calves were seen in SNEin contrast to Cape Cod Bay where calf sightingshave increased and up to 40 of the calves born in agiven year can be sighted (Mayo et al 2018)

Individual right whales were sighted more fre-quently in Cape Cod Bay than in SNE in the winterand spring and some whales move back and forthbetween the feeding habitats The relative impor-tance of the 2 areas for the whales is difficult toassess since differences in the frequency of apparenthabitat use are likely confounded by differences insurvey coverage Cape Cod Bay is a much smallerarea surrounded by land on 3 sides and comprehen-sive surveys are conducted weekly during the pri-mary period of right whale presence there betweenJanuary and April whereas SNE is an extensiveoceanic area and surveys were conducted only a fewtimes per month throughout the year

The year-round productivity of Nantucket Shoals(PCCS 2005) may influence the presence of rightwhales even in low numbers Indeed the shoalsappear to be a hotspot for right whales throughoutmost of the year The shoals extend eastward and

263

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Endang Species Res 45 251ndash268 2021

southeastward of Nantucket Island (Fig 1B Freire etal 2015) The shoals and Nantucket Sound form oneof the largest tidal dissipation areas in the Gulf ofMaine and New England regions (Chen et al 2018)The tidal dissipation creates a local tidal pump thatserves as the primary driver for the relatively highphytoplankton biomass in the shoalsrsquo shallow dune-like regions all year (Hu et al 2008 Saba et al 2015)which presumably correlates to zooplankton prey forright whales

In recent years right whale sightings in SNE watersin winter were concentrated in the eastern portion ofthe area near Nantucket Shoals and in and nearZones 6 and 7 of the Massachusetts wind energyarea In the spring right whale sightings in creased inthe northern parts of the wind energy areas andshifted generally westward but their specific loca-tions and extents varied with time Late spring aggre-gations of right whales were recently de tected outsideof the study area near the Ambrosendash Nantucket ship-ping lanes south of the Massachusetts wind energyareas (Fig 1B) by NEAq and NEFSC aerial surveysThis demonstrates that right whale aggregationsvary in space and time and can be formed in nearbylocations from which the whales could easily move tothe wind energy areas In recent summers rightwhale sightings increased in the Nantucket coastaland shoal waters but the observation efforts alsobecame more frequent Sightings in these Nantucketlocations were common in the summer of 2020 andextended into the early fall as suggested by observa-tions of right whales during the NEFSC surveys(NEFSC unpubl data) The 2019 and 2020 identifica-tions were unavailable at the time of our data re -quest but preliminary results suggest that a highnumber of juveniles were present in SNE waters atthis time in contrast to 2017 and 2018 (Quintana-Rizzo et al 2019ab) Additional data collection overthe coming years will reveal whether or not this pat-tern continues

The presence of right whales in SNE throughout allseasons is important to determine appropriate man-agement actions The study area is bracketed by 2right whale seasonal management areas (SMAs)these are regulatory protection zones along the USeast coast in which vessels larger than 300 gross tonsmust slow to 10 knots or less when transiting (NMFS2008) To protect aggregations of right whales outsideof the SMAs the National Marine Fisheries Servicehas voluntary dynamic management areas (DMAs)which are triggered when 3 or more whales aresighted within close proximity to each other DMAslast for 15 d from the date of the sighting(s) that trig-

gered them (NMFS 2008) It requests that ships avoidDMAs or transit through them at 10 knots or less Arecent assessment of the automatic identification sys-tem data of vessel traffic for these DMAs indicatesvery low mariner cooperation with speed reductionrequests (NMFS 2020) In 2017 and 2018 the annualnumber of DMAs doubled from the annual averageof 3 DMAs in the 2011minus 2016 period In 2019 the num-ber of triggered or extended DMAs reached a peakwith an active DMA in every month except October(NEFSC unpubl data)

The presence of right whales in SNE during all sea-sons is an important consideration for the planningand execution of offshore wind development Thehistorical seasonal migratory pattern should not beused alone to determine time-sensitive actions in thishabitat Monitoring and mitigation plans should in -clude protocols for the likely presence of right whalesthroughout the year (Whitt et al 2013) Their increas-ing summer and fall presence deserves special atten-tion since this will overlap with the current schedulefor pile driving for turbine foundations in the nextfew years the phase of construction considered tohave the greatest acoustic impact (Madsen et al2006 Thompson et al 2010) which could potentiallyaffect right whale behavior This timing was origi-nally selected based on the observed seasonality ofright whales in SNE (Leiter et al 2017) but our find-ings show that their seasonal occurrence has changedManagement and mitigation procedures should beadapted and reevaluated continually in relation toright whales use of the area

Although the effects of offshore wind energydevelopment on right whales are unknown it hasbeen reported that baleen whales avoid impulsivesounds with noise levels similar to those of pile-driving activities (Madsen et al 2006 Stone amp Tasker2006) Migrating baleen whales such as the bowheadwhale Balaena mysticetus a distant cousin of theright whale avoided airguns at approximately 20 km(Richardson et al 1999) Minke whales rapidly fleefrom military sonar exposures (Dolman amp Simmonds2010) and their numbers decline during naval activ-ity (Parsons et al 2000) The effects of noise associ-ated with vessel traffic during the construction andmaintenance of the wind turbines are also unclearbut right whales have not previously exhibited be -havioral responses to approaching vessels (Nowaceket al 2004) However analyses of right whale fecalsamples suggest that noise from large commercialvessels increases their stress levels (Rolland et al2012) Although right whales may be able to vocallyadapt to increased low-frequency noise to some

264

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Quintana-Rizzo et al Right whale wind energy areas

degree through a shift in vocalization frequency andduration (Parks et al 2007b 2009 2011) the abovefindings suggest that the whales could potentially benegatively affected by disturbances from sound andnoise related to wind energy development Increasedvessel traffic associated with the construction andmaintenance of turbines also increases the risk ofwhales being struck

Implementing mitigation measures by all lease-holding companies will be crucial The first leasingcompany to start pile-driving activities in the Massa-chusetts wind energy area has agreed to implementenhanced mitigation procedures to detect and pro-tect right whales from early winter to mid-May toavoid pile driving from January to April and to main-tain a comprehensive monitoring effort during theother months of the year that construction mighttake place (Vineyard Wind NGO Agreement 2019)Mitigation procedures will include using real-timeacoustic monitoring having certified protected spe-cies observers on a vessel stationed at the pile-drivingsite and using vessel surveys during daylight hourswithin a 10 km range of the construction site (Vine-yard Wind NGO Agreement 2019) However con-servation and management efforts will need to iden-tify specific indicators of potential impacts to reduceuncertainty especially as the offshore wind energyindustry grows and expands (Hill amp Arnold 2012Madsen et al 2015) Abundance and distributionstudies will not be enough to understand potentialchanges in right whale patterns considering the large-scale shifts that the species is experiencing Examplesof indicators exist in studies conducted in Europe(Koumlppel 2017 Bispo et al 2019) where wind energydevelopment has a long history Studies de signed toexamine the consequences of acoustic exposure toconstruction noise are urgently needed The area ofthe potential effect of acoustic exposure can extendfar beyond the immediate vicinity of the proposeddevelopment and cause behavioral disturbances inanimals in a large area (Thomsen et al 2006) Work isalso needed to determine if wind farms alter the habi-tatrsquos physical and oceanographic characteristics (Wil-helmsson et al 2006 Brostroumlm 2008 Paskyabi amp Fer2012 Paskyabi 2015 Carpenter et al 2016) This mayhave cascading impacts on the food chain in theregion which could potentially displace right whalesto other areas Estimating the potential impacts ofoffshore wind farms on right whales or their cause-and-effect relationships will be challenging at a timein which whale numbers and distributions are chang-ing but this is necessary to inform appropriate strate-gies for future wind energy development

Acknowledgements Funding for survey effort was providedby the Bureau of Ocean Energy Management under Cooper-ative Agreement M17AC00002 and the Massachusetts CleanEnergy Center (MassCEC) NEAq surveys were conductedunder NOAA permits no 14233 (2011minus2015) and no 19674(2017minus2019) issued to Scott D Kraus NOAA surveys wereconducted under research permits no 17355 June 2013minus June2018 and no 21371 after June 2018 NOAA Fisheries fundedthe publication of this paper The work includes data col-lected and processed by multiple institutions mdash our sincerethanks to the contributors of the North Atlantic Right WhaleConsortium and to the many observers who collected andprocessed sighting data at different organizations At NEAqwe acknowledge the work of A Bostwick J Anderson JTaylor S Mussoline K Stone and T Montgomery At NEFSCwe recognize the work of A Ogilvie J Gatzke K Vale CAccardo and K Slivka At CCS we thank A James L Gan-ley and P Hughes Surveys were possible with the coordina-tion of Avwatch in particular C Kluckhuhn T Laue R Jack-son B Strakele M Cortese and D Heikkila We thank DLeRoi for his technical assistance H Pettis P Hamilton andR Kenney provided helpful support during the data requestR Kenney calculated the survey effort of the aerial teamsworking in SNE M Zani was instrumental in identificationsand catalog work completed in 2011minus2015 J Roberts COrpha nides and an anonymous reviewer provided very use-ful comments to improve the manuscript EQR thanks NBolgen for his support D Engelhaupt for sharing informationon the movements of a tagged right whale H Whitehead forthe valuable discussions on the movement and residencemodels even in the middle of the pandemic and S Brillant AVanderlaan and M Smithson for insightful discussions in theearly stages of the manuscript This work is dedicated to theNorth Atlantic right whale

LITERATURE CITED

Baracho-Neto C Neto E Rossi-Santos M Wedekin L NevesM Lima F Faria D (2012) Site fidelity and residencetimes of humpback whales (Megaptera novaeangliae) onthe Brazilian coast J Mar Biol Assoc UK 92 1783minus1791

Berg J Hebblewhite M Clair CC Merrill E (2019) Preva-lence and mechanisms of partial migration in ungulatesFront Ecol Evol 7 325

Bispo R Bernadino J Coelho H Costa JL (eds) (2019) Windenergy and wildlife impacts Balancing energy sustain-ability with wildlife conservation Springer Cham

Brillant SW Vanderlaan ASM Rangeley RW Taggart CT(2015) Quantitative estimates of the movement and dis-tribution of North Atlantic right whales along the north-east coast of North America Endang Species Res 27 141minus154

Brostroumlm G (2008) On the influence of large wind farms onthe upper ocean circulation J Mar Syst 74 585minus591

Brown MW Fenton D Smedbol K Merriman C Robichaud-Leblanc K Conway JD (2009) Recovery strategy for theNorth Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Cagnacci F Focardi S Heurich M Stache A and others(2011) Partial migration in roe deer migratory and resi-dent tactics are end points of a behavioural gradientdetermined by ecological factors Oikos 120 1790minus1802

Carpenter JR Merckelbach L Callies U Clark S Gaslikova

265

Endang Species Res 45 251ndash268 2021

L Baschek B (2016) Potential impacts of offshore windfarms on North Sea stratification PLOS ONE 11 e0160830

Chabanne DBH Finn H Bejder L (2017) Identifying the rel-evant local population for environmental impact assess-ments of mobile marine fauna Front Mar Sci148

Chapman BB Broumlnmark C Nilsson JAring Hansson LA (2011)The ecology and evolution of partial migration Oikos120 1764minus1775

Chapman BB Hultheacuten K Brodersen J Nilsson PA Skov CHansson LA Broumlnmark C (2012) Partial migration infishes causes and consequences J Fish Biol 81 456minus478

Charif RA Shiu Y Muirhead CA Clark CW Parks SE RiceAN (2020) Phenological changes in North Atlantic rightwhale habitat use in Massachusetts Bay Glob ChangeBiol 26 734minus745

Chen Z Curchitser E Chant R Kang D (2018) Seasonal vari-ability of the cold pool over the Mid-Atlantic Bight conti-nental shelf J Geophys Res C Oceans 123 8203minus8226

Cole TVN Hamilton P Henry AG Duley P Pace RM IIIWhite BN Frasier T (2013) Evidence of a North Atlanticright whale Eubalaena glacialis mating ground EndangSpecies Res 21 55minus64

Cooke JG (2020) Eubalaena glacialis The IUCN Red List ofThreatened Species 2020 eT41712A162001243 https dx doiorg102305IUCNUK2020-2RLTS T41712 A16200 1243 en (accessed 24 Nov 2020)

Corkeron P Hamilton P Bannister J Best P and others (2018)The recovery of North Atlantic right whales Eubala enaglacialis has been constrained by human-caused mortal-ity R Soc Open Sci 5 180892

Davies KTA Brillant SW (2019) Mass human-caused mortal-ity spurs federal action to protect endangered NorthAtlantic right whales in Canada Mar Policy 104 157minus162

Davies KTA Vanderlaan ASM Smedbol RK Taggart CT(2015) Oceanographic connectivity between right whalecritical habitats in Canada and its influence on whaleabundance indices during 1987minus2009 J Mar Syst 150 80minus90

Davies KTA Brown MW Hamilton PK Knowlton AR Tag-gart CT Vanderlaan ASM (2019) Variation in NorthAtlantic right whale Eubalaena glacialis occurrence inthe Bay of Fundy Canada over three decades EndangSpecies Res 39 159minus171

Davis GE Baumgartner MF Bonnell JM Bell J and others(2017) Long-term passive acoustic recordings track thechanging distribution of North Atlantic right whales(Eubalaena glacialis) from 2004 to 2014 Sci Rep 7 13460

Deakos MH Baker JD Bejder L (2011) Characteristics of amanta ray Manta alfredi population off Maui Hawaiiand implications for management Mar Ecol Prog Ser429 245minus260

Dinis A Alves F Nicolau C Ribeiro C Kaufmann MCantildeadas A Freitas L (2016) Bottlenose dolphin Tursiopstruncatus group dynamics site fidelity residency andmovement patterns in the Madeira Archipelago (North-East Atlantic) Afr J Mar Sci 38 151minus160

Dolman S Simmonds M (2010) Towards best environmen-tal practice for cetacean conservation in developingScotlandrsquos marine renewable energy Mar Policy 34 1021minus1027

Firestone J Lyons SB Wang C Corbett JJ (2008) Statisticalmodeling of North Atlantic right whale migration alongthe mid-Atlantic region of the eastern seaboard of theUnited States Biol Conserv 141 221minus232

Fisheries and Oceans Canada (2014) Recovery strategy for

the North Atlantic right whale (Eubalaena glacialis) inAtlantic Canadian waters Species at Risk Act recoverystrategy series Fisheries and Oceans Canada Ottawa

Foley HJ Holt RC Hardee RE Nilsson PB and others (2011)Observations of a western North Atlantic right whale(Eubalaena glacialis) birth offshore of the protected south-east US critical habitat Mar Mamm Sci 27 E234minusE240

Frasier TR Hamilton PK Brown MW Conger LA and others(2007) Patterns of male reproductive success in a highlypromiscuous whale species the endangered NorthAtlantic right whale Mol Ecol 16 5277minus5293

Freire R Persquoeri S Madore B Rzhanov Y Alexander L ParrishCE Lippmann TC (2015) Monitoring near-shore bathy -metry using a multi-image satellite-derived bathymetryapproach US Hydrographic Conference 2015

Ganley LC Brault S Mayo CA (2019) What we see is notwhat there is estimating North Atlantic right whaleEubalaena glacialis local abundance Endang SpeciesRes 38 101minus113

Getis A Ord JK (1992) The analysis of spatial association byuse of distance statistics Geogr Anal 24 189minus206

Gowan TA Ortega-Ortiz JG Hostetler JA Hamilton PK andothers (2019) Temporal and demographic variation inpartial migration of the North Atlantic right whale SciRep 9 353

Hamilton PK Marx MK Kraus SD (1995) Weaning in NorthAtlantic right whales Mar Mamm Sci 11 386minus390

Hamilton PK Knowlton AR Marx MK (2007) Right whalestell their own stories the photo-identification catalog In Kraus SD Rolland RM (eds) The urban whale NorthAtlantic right whales at the crossroads Harvard Univer-sity Press Cambridge MA p 75minus104

Hatch LT Clark CW Van Parijs SM Frankel AS PonirakisDW (2012) Quantifying loss of acoustic communicationspace for right whales in and around a US national mar-ine sanctuary Conserv Biol 26 983minus994

Hill D Arnold R (2012) Building the evidence base for eco-logical impact assessment and mitigation J Appl Ecol496ndash9

Hu SD Townsend W Chen C Cowles G Beardsley RCRubao J Houghton RW (2008) Tidal pumping and nutri-ent fluxes on Georges Bank a process-oriented model-ing study J Mar Syst 74 528minus544

IWC Int (International Whaling Commission) (2001) Reportof the workshop on the comprehensive assessment of rightwhales a worldwide comparison J Cetacean Res Manag1ndash35 Available at httpsjournaliwcint index phpjcrm articleview270

Kenney RD (2019) The North Atlantic Right Whale Consor-tium database a guide for users and contributors ver-sion 6 North Atlantic Right Whale Consortium Ref Doc2019-02 University of Rhode Island Narragansett RI

Khan C Cole T Duley P Henry A Gatzke J (2011) NorthAtlantic right whale sighting survey (NARWSS) and rightwhale sighting advisory system (RWSAS) 2010 resultssummary US Dep Commer Northeast Fish Sci Cent RefDoc 11-05

Knowlton AR Kraus SD Kenney RD (1994) Reproduction inNorth Atlantic right whales (Eubalaena glacialis) Can JZool 72 1297minus1305

Koumlppel J (2017) Wind energy and wildlife interactions Presen-tations from the CWW2015 conference Springer Cham

Kraus SD Hatch JJ (2001) Mating strategies in the NorthAtlantic right whale (Eubalaena glacialis) J CetaceanRes Manag Spec Issue 2 237minus244

266

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Kraus SD Rolland RM (2007) The urban whale syndromeIn Kraus SD Rolland RM (eds) The urban whale NorthAtlantic right whales at the crossroads Harvard Univer-sity Press Cambridge MA p 488minus513

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Editorial responsibility Ana Cantildeadas Durham North Carolina USA

Reviewed by J Roberts and 1 anonymous referee

Submitted January 3 2021Accepted May 27 2021Proofs received from author(s) July 13 2021