urban forests sustain diverse carrion beetle …urban forests sustain diverse carrion beetle...

Submitted 3 October 2016Accepted 14 February 2017Published 15 March 2017

Corresponding authorJason Munshi-Southjasonnycevolutionorgjmunshisouthfordhamedu

Academic editorNathan Sanders

Additional Information andDeclarations can be found onpage 17

DOI 107717peerj3088

Copyright2017 Fusco et al

Distributed underCreative Commons CC-BY 40

OPEN ACCESS

Urban forests sustain diverse carrionbeetle assemblages in the New York Citymetropolitan areaNicole A Fusco1 Anthony Zhao2 and Jason Munshi-South1

1 Louis Calder CenterndashBiological Field Station Fordham University Armonk NY USA2Department of Entomology University of Maryland at College Park College Park MD USA

ABSTRACTUrbanization is an increasingly pervasive form of land transformation that reducesbiodiversity of many taxonomic groups Beetles exhibit a broad range of responses tourbanization likely due to the high functional diversity in this order Carrion beetles(Order Coleoptera Family Silphidae) provide an important ecosystem service bypromoting decomposition of small-bodied carcasses and have previously been foundto decline due to forest fragmentation caused by urbanization However New YorkCity (NYC) and many other cities have fairly large continuous forest patches thatsupport dense populations of small mammals and thus may harbor relatively robustcarrion beetle communities in city parks In this study we investigated carrion beetlecommunity composition abundance and diversity in forest patches along an urban-to-rural gradient spanning the urban core (Central Park NYC) to outlying rural areasWe conducted an additional study comparing the current carrion beetle communityat a single suburban site in Westchester County NY that was intensively surveyed inthe early 1970rsquos We collected a total of 2170 carrion beetles from eight species at 13sites along this gradient We report little to no effect of urbanization on carrion beetlediversity although two species were not detected in any urban parks Nicrophorustomentosus was the most abundant species at all sites and seemed to dominate theurban communities potentially due to its generalist habits and shallower burying depthcompared to the other beetles surveyed Variation between species body size habitatspecialization and forest area surrounding the surveyed sites also did not influencecarrion beetle communities Lastly we found few significant differences in relativeabundance of 10 different carrion beetle species between 1974 and 2015 at a singlesite in Westchester County NY although two of the rare species in the early 1970rsquoswere not detected in 2015 These results indicate that NYCrsquos forested parks have thepotential to sustain carrion beetle communities and the ecosystem services they provide

Subjects Biodiversity Conservation Biology Ecology EntomologyKeywords Carrion beetles New York City Urban parks Urbanization Urban ecology Silphidae

INTRODUCTIONThe ecological influence of urbanization is increasingly pervasive around the world In2014 54 of the worldrsquos human population resided in urban areas (United Nations 2014)and urban populations increased by 12 between 2000 and 2010 in the United States(United States Census Bureau 2010) Urban landscapes are highly modified for human

How to cite this article Fusco et al (2017) Urban forests sustain diverse carrion beetle assemblages in the New York City metropolitanarea PeerJ 5e3088 DOI 107717peerj3088

use with natural habitats typically occurring only in small fragmented patches (SaundersHobbs amp Margules 1991) Fragmentation in cities often decreases species richness changescommunity composition and alters ecosystem processes (Didham 2010) Many speciesare impacted negatively by urbanization (carnivoresmdashOrdentildeana et al 2010 arthropodsmdashSattler et al 2010 amphibiansmdashHamer amp Parris 2011 birds amp plantsmdashAronson et al2014) but effects vary based on the taxonomic group in question (McKinney 2008) Forexample studies of arthropod diversity along urban-to-rural gradients have documenteda wide variety of responses to urbanization (Hornung et al 2007 Niemelauml amp Kotze2009 Varet Peacutetillon amp Burel 2011 Magura Nagy amp Tothmeresz 2013 Savage et al 2015Diamond et al 2015) Given the extreme variety of life history traits and habitat use amongarthropods responses to urbanization may be difficult to predict

Carrion beetles use small mammal carcasses as food sources for their young (Scott 1998)These beetles bury carcasses to avoid competition with other scavengers thus facilitatingdecomposition and providing considerable ecosystem services Availability of carrionlikely influences the abundance and diversity of carrion beetles Carrion beetle speciescompete with each other as well as with other scavenging vertebrates (Scott 1998 Trumboamp Bloch 2000 DeVault et al 2011) and invertebrates for this resource (Ratcliffe 1996Gibbs amp Stanton 2001) Urbanization alters natural habitats in myriad ways (Grimm et al2008) that may cause local extirpations or reduced abundance of native small mammals(eg likely carrion) and carrion beetles in cities

Gibbs amp Stanton (2001) previously reported that forest fragmentation reduced carrionbeetle species richness and abundance in Syracuse New York Beetles that persisted in thesefragments were primarily small-bodied habitat generalists and other carrion beetles mayhave declined in abundance due to lower carcass availability increased prevalence of otherscavengers or reduced soil and litter quality Wolf amp Gibbs (2004) also found that forestfragmentation decreased carrion beetle diversity and abundance in Baltimore MarylandThey argued that forest contiguity was an important factor affecting richness abundanceand diversity of carrion beetles in this city However these studies did not directly addresswhether large parks within core urban areas harbor a substantial diversity of carrion beetles

In this study we investigated species richness diversity relative abundance and com-munity similarity of carrion beetles (Family Silphidae) across an urban-to-rural gradientin the New York City (NYC) metropolitan area NYC is the most densely populated areain North America but 27 of the cityrsquos land area is comprised of vegetated natural areasparticularly within several large urban parks (New York City Department of City Planning2002) These parks are characterized by substantial forest cover and high densities of smallmammals (Munshi-South amp Kharchenko 2010) and thus may provide high-quality habitatfor a diverse assemblage of carrion beetles Alternatively NYCrsquos urban forests may harborless carrion beetle diversity relative to suburban and rural areas outside of NYC as wasfound in Baltimore and Syracuse (Gibbs amp Stanton 2001 Wolf amp Gibbs 2004) We alsocompared historical records from a single site (Pirone amp Sullivan 1980) the Louis CalderCenter in Armonk New York with our 2015 estimates of carrion beetle diversity andabundance to examine changes over the last four decades The forest area at the LouisCalder Center has not changed in that time but urbanization of the surrounding area and

Fusco et al (2017) PeerJ DOI 107717peerj3088 222

Table 1 Characteristics classification and quantification of urbanization at each sample sites along with species richness and species diversitymeasures at each site (urban= orange suburban= teal rural= purple)

Site code Site name Siteclassification

Meanimpervioussurface

Species Richness(species number)

Species Diversity(Simpsonrsquos 1D)

NYBG New York Botanical Garden Urban 6088 2 161HBP High Bridge Park Urban 6054 6 184CP Central Park Urban 6024 6 266IHP Inwood Hill Park Urban 2997 6 294VCP Van Cortlandt Park Urban 2797 5 234SWP Saxon Woods Park Suburban 1763 5 237LCC Louis Calder Center Suburban 1057 ndash ndash

LCC1 Louis Calder Center Sample 1 ndash ndash 3 320LCC2 Louis Calder Center Sample 2 ndash ndash 4 259LCC3 Louis Calder Center Sample 3 ndash ndash 5 287

CSH Convent of Sacred Heart Suburban 1114 4 231RSP Rockefeller State Park Suburban 474 5 175MRG Mianus River Gorge Preserve Suburban 064 6 259CT Western Connecticut Rural 089 3 238CAT Catskills Rural 046 5 168CFP Clarence Fahnestock State Park Rural 020 4 177

a rapid increase in deer herbivory may have resulted in altered diversity of communitycomposition of carrion beetles

Urban forests have the potential to harbor substantial biodiversity in cities worldwide(Faeth Bang amp Saari 2011 Elmqvist et al 2013 La Sorte et al 2014 Aronson et al 2014)Diamond et al (2015) argued that increases in biodiversity may be due to introduction ofnon-native species as well as increased habitat heterogeneity in densely populated areasbut many native species still persist in these urban remnants Urban carrion beetle diversitythat rivals surrounding rural areas would indicate that urban forests in NYC currentlyprovide ample habitat and resources to sustain these native beetle communities

MATERIALS amp METHODSStudy site and sampling techniquesThis study was conducted across an urban-to-rural gradient spanning 120 km from theurban core of NYC (Central Park Manhattan) to southern New York State and westernConnecticut Carrion beetles were collected from five urban sites in New York City fivesuburban sites and three rural sites (Table 1 and Fig 1) Urban suburban and ruralsite classifications followed Munshi-South Zolnik amp Harris (2016) and were based onpercent impervious surface cover Many of our sampling sites were previously used byMunshi-South Zolnik amp Harris (2016) to examine population genomics of white-footedmice (Peromyscus leucopus) and thus classifications were already available For sites uniqueto this study we used the same methods to quantify urbanization (Table 1 and Fig 1) Inbrief we created 2 km boundary buffers around our study sites in ArcGIS 103 (ESRI 2014)


CP

CT

CFP

CSH

CAT

RSP

HBPIHPVCP

SWP

LCCMRG

NYBGUuml 0 10 205 Kilometers

State LineSite Points

2000m Site BufferUrbanSuburbanRural

Landcover0 Impervious SurfaceWater

Impervious Surface100501

Figure 1 Geographic location of study sites surrounded by 2 km buffer circles Urban (orange) sub-urban (teal) and rural (purple) sites were classified according to impervious surface in these buffersas described in the textGreen areas represent no impervious surface whereas areas of increasing pinkcoloration denote increasing percent impervious surface as reported in the 2011 National LandcoverDatabase (Xian et al 2011) Site abbreviations follow Table 1

and then used zonal statistics to calculatemean percent impervious surface from the PercentDeveloped Imperviousness data layer imported from the National Land Cover Database2011 (Xian et al 2011)

For comparison with previous carrion beetle surveys in other cities we followed thesampling methods and trap design employed by Gibbs amp Stanton (2001) andWolf amp Gibbs(2004) We constructed traps from open-topped cylinders by cutting the top off 1 L plasticbottles adding a loop of string to hang the trap and attaching a rain cover (cardboardcovered in plastic cling wrap) by threading it through the string Most traps contained 200mL of a 11 mixture of ethylene glycol and water although soapy water was substituted atthe Manhattan sites due to public safety regulations A small glass jar containing bait (sim65cm2 of rotting chicken thigh) was topped with a punctured lid to prevent insects fromdestroying the bait but permitting odors to attract carrion beetles This jar was placed insideeach plastic trap that was then filled with the ethylene glycol mixture We set three traps ateach site close to forest edges and at least 100 m apart Traps were hung from small treebranches approximately 1ndash15 m from the ground to prevent other wildlife from disturbingthe traps Traps were set out for seven consecutive days at each site where beetles were


collected upon the last day We conducted all trapping from 22 June to 05 August 2015At each study location we separated beetles from other insects and stored beetles in 80ethanol before bringing all specimens to the laboratory for identification We identified allcarrion beetle species following Hanley amp Cuthrell (2008) After collection all beetles werestored in ethanol at minus20 C Permission to collect carrion beetles was granted by the NewYork City Department of Parks and Recreation the Rockefeller State Park Preserve andthe Connecticut Department of Energy and Environmental Protection (Permit number1214008)

Relative abundance at urban suburban and rural sitesTo describe variation among sites and site classes we calculated relative abundance as theproportion of each species compared to the total number of individuals at each site Toexamine changes over the summer season in carrion beetle diversity and relative abundanceat the Louis Calder Center (a suburban site) we conducted three separate trapping surveysfrom 22ndash29 June 14ndash21 July and 22ndash29 July 2015 Only data collected from the thirdsurvey were used in the main urban-to-rural analysis to more accurately compare tosamples taken during the same time period as sampling at the other sites (mid to late July2016) We calculated the relative proportion of each species for each of the three surveysat the Louis Calder Center to examine changes throughout the study period

Historical comparison of carrion beetle presence and abundancePirone amp Sullivan (1980) performed carrion beetle sampling at the Louis Calder Centerin Armonk NY for an 8-month period (AprilndashNovember) in 1974 They collected 4300silphid beetles in 6 pitfall traps Although our current study is only a snapshot (3 weeksof sampling) of the current community assembly at this site the current data collected in2015 from all three surveys at the Louis Calder Center (JunendashJuly) were used to comparethe current carrion beetle species (2015) with the species observed in the historical study(1974) A studentrsquos t -test was conducted to compare total relative abundance in 1974ndash2015

Species diversity and species richness along an urban-to-ruralgradientTo determine whether our sample size was robust enough for running subsequent statisticalanalyses we performed a rarefaction analysis for all sites in R v323 (R Core Team 2015)using the vegan package For the analysis along the urban-to-rural gradient we used twodifferent measures species richness and species diversity To compare species diversityacross sites we calculated the Simpsonrsquos reciprocal index (1D Simpson 1949) of diversityWe also calculated other diversity indices for comparison (equations Jost 2006 Table S1)These results showed similar trends across sites for all indices therefore we chose to use thevery commonly used Simpsonrsquos reciprocal index for statistical analyses We then calculatedcommunity similarity using the Jaccard Index of community similarity (Jaccard 1901)

CCJ= SJ= a(a+b+ c)

where SJ is the Jaccard similarity coefficient a is the number of species shared by all sitesb is the number of species unique to the first site and c is the number of species unique to


the second site Then we calculated the Jaccard coefficient of community similarity for allthe data pooled across sites classes (urban suburban and rural) to analyze overall carrionbeetle community assemblages Lastly we conducted a hierarchical cluster analysis usingthe betapart package in R (Baselga amp Orme 2012) to explore patterns of beta diversitypartitioning this diversity measure into the nestedness and the turnover components

To examine the influence of urbanization on species richness and diversity we calculatedgeneral linear regressions of mean percent impervious cover versus species richness andspecies diversity at each site using RWe also calculated a general linear regression to explorethe difference in relative abundance of the most abundant species Nicrophorus tomentosusversus mean percent impervious surface at all sites Additionally we performed a gradientanalysis by creating a Non-metric Multidimensional Scaling (NMDS) plot using the Veganpackage (Oksanen et al 2016) in R to investigate population dissimilarity based on site class(urban suburban and rural) NMDS compares species changes from one community tothe next by using rank order comparison and calculates the pairwise dissimilarity of pointsin low-dimensional space (Buttigieg amp Ramette 2014) Thus NMDS allows us to robustlyestimate dissimilarity between site locations based on the type of site and the specieslocated in each site

Species-specific differences across urban suburban and rural sitesMany studies on beetles have focused on specific characteristics that may underlie differ-ences in species richness and diversity within sites and across studies (Davies amp Margules2000) We conducted a factorial ANOVA to examine the interaction effect of species bodysize (small lt 5 mm medium = 5ndash65 mm large gt 65 mm estimations and groupingsbased on data from Gibbs amp Stanton 2001) and site classification (urban suburban rural)based on relative abundance We also used a Studentrsquos t -test to examine relative abundancewhen species are classified as habitat generalists versus habitat specialists (Gibbs amp Stanton2001) Lastly we performed a general linear regression to explore if a relationship existsbetween species richness or species diversity and the forest area () existing at eachsite At each site the forest area was calculated using the Tabulate Area tool from theArcGIS 103 (ESRI 2014) Toolbox to calculate the forest area within the same 2 km bufferssurrounding each site as was used to calculate percent impervious surface We then calcu-lated the relative proportion of forest area compared to the total area within the buffer Weused forest area data from the USGS National Landcover Dataset (Homer et al 2011)

RESULTSRelative abundance at urban suburban and rural sitesWe collected a total of 2170 carrion beetles comprising eight silphid species (Table 2)across all sites (Table 1 Fig 1) Nicrophorus tomentosus was the most abundant at allsites accounting for 568 of all beetles captured (Fig 2) yet there was no significantrelationship between Ni tomentosus relative abundance and percent mean impervioussurface of each site (F(210)= 116 pgt 005) Other species also varied in presence orabundance between urban suburban and rural forests (Fig 2) specifically Oiceoptomanoveboracense was capturedmore often in suburban areas (235) and urban areas (219)


Table 2 Abundance data for eight carrion beetle (Family Silphidae) species at all site locations (site abbreviations and classification found in Table1)

Species Nicrophorusorbicollis

Nicrophorustomentosus

Nicrophorusdefodiens

Nicrophoruspustulatus

Nicrophorussayi

Oiceoptomainaequale

Oiceoptomanoveboracense

Necrophilaamericana

NYBG 50 165 1 8 0 25 77 0HBP 3 28 0 0 0 1 7 0CP 0 6 0 0 0 0 19 0IHP 61 70 1 1 0 1 20 0VCP 22 75 0 1 0 3 75 0SWP 7 87 0 15 0 1 125 0LCC 39 257 0 3 0 0 55 41

LCC1 8 54 0 0 0 0 28 9LCC2 26 168 0 1 0 0 7 25LCC3 5 35 0 2 0 0 20 7

CSH 50 182 2 0 0 0 11 53RSP 17 90 0 0 0 0 74 0MRG 26 221 35 0 0 0 6 4CT 1 97 0 0 0 0 15 20CAT 63 106 0 5 7 0 2 17CFP 50 165 1 8 0 25 77 0

than at rural sites (16) whereas Nicrophorus defodiens was captured predominantly inrural areas (71) versus urban areas (03) and suburban areas (02) SimilarlyNecrophila americana was recorded in suburban (84) and rural areas (43) but was notfound in any urban sites Nicrophorus sayi was only recorded at one rural park accountingfor 14 of the total number of beetles captured at rural sites (Tables 1 and 2 and Fig 2)

Historical comparison of carrion beetle presence and abundanceWe captured 358 individuals cumulatively across three surveys at the Louis Calder Centerthroughout summer 2015 Five carrion beetle species were observed at Louis CalderCenter with the absence of Ni defodiens Ni sayi and Oiceoptoma inaequale found at othersuburban and rural sites Nicrophorus pustulatus and Necrophila americana were absentfrom the first surveys and appeared in later surveys Ni tomentosus became more prevalent(344 545 740) throughout the summer andO noveboracense decreased in relativeabundance (344 283 31 Fig 3)

Results of carrion beetle observations at the Louis Calder Center site show a smallreduction in species richness 7 species in 1974 to 5 species in 2015 (Fig 3) Ni defodiensNi sayi and O inaequale were absent both historically and currently at this site yet werepresent at other suburban sites The two species not observed in 2015 that were already


0

25

50

75

100

Ni

orb

ico

llis

Ni

tom

en

tosu

s

Ni

de

fod

ien

s

Ni

pu

stu

latu

s

Ni

sayi

O in

eq

ua

le

O n

ove

bo

race

nse

Ne a

me

rica

na

Species

Re

lativ

e A

bu

nd

an

ce

(

)

Site Classification

Urban

Suburban

Rural

Figure 2 Relative abundance () of species across site classes urban (orange) suburban (teal) ru-ral (purple) sites Bold lines within the boxes indicate the median value the colored boxes represent theinter-quartile range (Quartile 1ndashQuartile 3) the whiskers extend 15 IQR and the dots represent outliervalues

low in relative abundance in 1974 were Necrodes surinamensis (02) and Necrophiluspettiti (03 Fig 4) There was no significant difference in the relative abundance ofspecies in 1974 to 2015 (t (9)= 0546 p= 0599) The 2015 data show an increasing trendin the relative abundance of Ni tomentosus (58ndash543) in 1974 versus 2015 and adecreasing trend in the relative abundance of Necrophila americana (418ndash67) andO noveboracense (38ndash219) since 1974 (Fig 4)

Species diversity and species richness along an urban-to-ruralgradientAcross the urban-to-rural gradient there was no significant relationship between meanpercent impervious surface of a site and carrion beetle species richness (R2

= 0028 pgt

005) or species diversity (R2= 00213 pgt 005) However NMDS ordination plots exhibit

dissimilarity in carrion beetle assemblages in rural and urban sites NMDS also showedthat beetle assemblages in suburban sites were more similar to those in the urban sitesBased on the size of the convex hulls heterogeneity of carrion beetle species compositionwas the greatest for suburban sites and least for urban sites (Fig 5)


Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species

Late JuneMid JulyLate July

Figure 3 Relative abundance () of species across three sampling surveys (Late June Mid July Late July)at the Louis Calder Center site in Armonk NY

We observed relatively high community similarity indices across most pairwisecomparisons (CCj = 0333ndash1000 Table 3) Several pairs of nearby sites had very highcommunity similarity such as two urban sites Inwood Hill Park and New York BotanicalGarden (CCj = 1000) and two suburban sites Convent of the Sacred Heart School andLouis Calder Center (CCj = 1000) The most distant pairs of sites were less similar mostnotably between highly urbanized Central Park and rural Clarence Fahnestock State Park(CCj = 0333) The pooled urban carrion beetle community was more similar to the pooledsuburban community (CCj = 0857) than to the pooled rural community (CCj = 0750)as also demonstrated in the NMDS ordination (Fig 5) The pooled rural community wasequally similar to both the pooled urban and suburban communities (CCj = 0750) Thenestedness component of beta diversity in the hierarchical cluster analysis clustered sitesbased on species richness trends not based on site classifications (Fig 6A) Alternativelythe hierarchical clustering of the turnover component clusters all urban sites togetherwith a few suburban sites in one branch and all rural sites and the other suburban sites inanother cluster (Fig 6B) as reflected by the results of the NMDS plot (Fig 5)


Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Ne

pet

titi

Ne

sur

anam

ensi

s

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species

LCC 1974LCC 2015

Figure 4 Relative abundance of species at the Louis Calder Center site in 1974 (Pirone amp Sullivan 1980)and in 2015

Table 3 Pairwise Jaccard community similarity index values calculated between all sample sites (site abbreviations and classification located inTable 1)

NYBG HBP CP IHP VCP SWP LCC CSH RSP MRG CT CAT CFP

NYBG ndash 0667 0333 1000 0833 0833 0571 0571 0571 0500 0571 0625 0500HBP ndash 0500 0667 0800 0800 0500 0500 0500 0750 0500 0750 0429CP ndash 0333 0400 0400 0400 0400 0400 0667 0400 0500 0333IHP ndash 0833 0833 0571 0571 0571 0500 0571 0750 0500VCP ndash 1000 0667 0667 0429 0600 0429 0875 0571SWP ndash 0667 0667 0429 0600 0429 0875 0571LCC ndash 1000 0667 0600 0667 0875 0833CSH ndash 0667 0600 0667 0571 0833RSP ndash 0600 1000 0625 0833MRG ndash 0600 0875 0500CT ndash 0875 0600CAT ndash 0875CFP ndash


minus05 00 05

minus06

minus04

minus02

00

02

04

NMDS1

NMDS2

CP

CFP

SWP

CATCT

NYBG

RSP

LCC

IHP

MRG

VCP

HBPCSH

Figure 5 Non-metric multidimensional scaling (NMDS) of abundance of carrion beetle species at eachsite grouped by site class as a convex hull

Species-specific differences across urban suburban and rural sitesWe found no significant effect between beetle body size and site class (urban suburbanrural) for relative abundance of carrion beetle species in this study Additionally whenfocusing on habitat specialization we also found no significant difference in habitatspecialization betweenurban suburban and rural sites (Table S1) Lastly we foundno trendin species richness (Fig S1A) or species diversity (Fig S1B) across increasing continuousforest areas throughout sampled sites

DISCUSSIONContrary to our predictions we observed few differences in beetle diversity or richnessalong an urban-to-rural gradient in the NYCmetropolitan area Along this gradient urbanand suburban sites were nearly equally diverse and species-rich as rural sites We alsodetected little to no influence of urbanization (measured by mean percent impervioussurface) on relative species abundance species diversity or species richness of carrionbeetles throughout these sites Although species richness is not very high we observedrelatively high carrion beetle community similarity values betweenmost pairs of sites in thisstudy regardless of their urbanization status (Jaccard Index= 0333ndash1000 Table 3) Whenpartitioning beta diversity nestedness follows species richness trends further strengtheningthe result that there is no difference in carrion beetle communities between urban suburban


MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)

Figure 6 Hierarchical cluster analysis of sites (abbreviations found in Table 1) based on (A) the turnovercomponent and (B) the nestedness component of the Jaccard Similarity Index for beta diversity


and rural classified sites Alternatively turnover may be driven by site class based onurbanization to some extent

Overall even with limited sampling this study demonstrates that a diverse communityof carrion beetles are able to thrive in rural suburban and urban forests in and aroundNew York City Gibbs amp Stanton (2001) and Wolf amp Gibbs (2004) reported that carrionbeetle diversity is significantly reduced around Syracuse NY and Baltimore MD due toforest fragmentation associated with urbanization but our results indicate that forestedcity parks in the most urbanized areas of North America (ie Manhattan and the BronxNYC) do harbor substantial carrion beetle diversity compared to surrounding rural areasWe did not directly examine variation in fragment size within urban suburban and ruralareas but the discrepancy between these earlier results and ours may be due to the fact thaturban forests in NYC parks are relatively large compared to other cities

Arthropods have exhibited highly variable even dichotomous responses to urbanizationaround the world (Lessard amp Buddle 2005 Sattler et al 2010) Other studies show that theinfluence of urbanization varies based on taxonomic group geographic location climateand spatial scale (McKinney 2008 Kotze et al 2011 Martinson amp Raupp 2013) Carabidbeetles are the most well-studied arthropod group carabid species richness has been foundto decrease (Gaublomme et al 2008) or not change (Deichsel 2006) in urban areas In areview of carabids and urbanization Magura Lovei amp Tothmeresz (2010) argued that thisvariation was due to site-specific effects operating in each study Urbanization did nothomogenize carabid assemblages in cites in England Denmark and Helsinki Finlandbut urbanization did affect species assemblages in other Finnish cities Hungary Japanand Bulgaria (Kotze et al 2011) Other than location discrepancies across studies maybe related to the choice of variables for analysis Differing climates different measures ofurbanization (eg human population density economics housing density or impervioussurface) different times of the year studies were conducted and spatial scale (Faeth Bangamp Saari 2011) all could affect species presence richness and diversity results in urbanareas Although carrion beetles may not be representative of all arthropod species thesesame factors may also explain some of the differences between the NYC results presentedhere and those of Gibbs amp Stanton (2001) and Wolf amp Gibbs (2004) for Syracuse NY andBaltimore MD

When quantifying and classifying urbanization many studies use measures basedon forest fragmentation extent of forest cover isolation caused by human-induceddisturbance impervious surface or human population density (McDonnell amp Hahs 2008)The use of a common index to represent urbanization is necessary to compare results acrossstudies but there are no common indices currently in wide useMcDonnell amp Hahs (2008)and Kotze et al (2011) stress the need for such commonmeasures to examine the generalityof the influence of urbanization on biodiversity patterns Comparing our study to othercarrion beetle studies we used mean percent impervious surface to quantify urbanizationwhereasGibbs amp Stanton (2001)Wolf amp Gibbs (2004) and Klein (1989) utilized continuousforest cover and fragmentation to classify the level of urbanization at each site Our studyspecifically quantified urbanization with mean percent impervious surface using 2 kmbuffers as was previously reported byMunshi-South Zolnik amp Harris (2016) formany of the


same study sites Although many metrics can be employed to measure urbanization webelieve that impervious surface cover is particularly useful for urban-to-rural gradientstudies because it is measurable for nearly any terrestrial area and directly related to urbanlandscape modification

We also examined species relative abundance changes over three sampling periods at asuburban site the Louis Calder Center in Westchester County NY Despite no significantchange in total abundance across samples throughout the summer season we did see slightchanges in species abundance over different collection periods (Fig 3) In comparisonto Wolf amp Gibbs (2004) our study showed opposite trends in species presence across thecollection period This difference could be due to difference in climate and temperatureacross June July and August in NYC versus the more southern Baltimore MD InArmonk NY Ni tomentosus O noveboracense and O inaequale were more abundantlater in the summer and Ni orbicollis was more abundant earlier in the summer Scott(1998) describesNi tomentosus as a late summer early fall breeder whichwas corroboratedby our observation that Ni tomentosus was most abundant in the latest summer surveyNi orbicollis begins breeding in late spring (Ratcliffe 1996) and was the most abundant inour first sample session at this site Ni sayi is most active in very early spring which mayexplain the absence of this species at this site during the summer Lastly the absence ofNi pustulatusmay be due to their habitat preference for wetlands (Gibbs amp Stanton 2001)which were not very extensive around our trap sites in this study

Species richness of carrion beetles did not differ greatly between 1974 and 2015 at theLouis Calder Center site However we did record pronounced species-specific differencesin abundance between the past study (Pirone amp Sullivan 1980) and this current study in2015 (Fig 4) Species differences over time could be due to anthropogenic modification ofthe landscape in and around the Louis Calder Center site since the early 1970s There wasan increase in human population density in the town of North Castle NY in WestchesterCounty from 9591 (1970) to 11841 (2010) according to the Decennial Census 1950ndash2010(United States Census Bureau 2010) An increase in population density often results inconstruction of more housing and roads and subsequent fragmentation of forests whichcould alter current species assemblages We identified the most drastic change in relativeabundance over time for three species Ni tomentosus O noveboracense and Necrophilaamericana (Fig 4) In contrast relative abundance of Ni tomentosus increased whichcould be due to the fact that this species is an ecological generalist that becomes morecommon after habitat degradation There was a substantial decrease in O noveboracensesince 1974 Since univoltine arthropod species are more affected by habitat loss (Kotzeet al 2011) the reduction in O noveboracense may be due to their inability to effectivelycompete with multivoltine species as well as their limited dispersal ability in warmertemperatures (Ratcliffe 1996) Lastly the most drastic decline was inNecrophila americanawhich is perhaps due to its large body size (smaller bodied generalists can survive in moredisturbedurban habitat Gibbs amp Stanton 2001 Elek amp Loumlvei 2007) and its preferencefor field habitat (Ratcliffe 1996) which may be more limited in the area in 2015 due tofragmentation and the reduction in agriculture Two previously-observed speciesNecrodessurinamensis and Necrophilus pettiti were completely absent in our contemporary sample


Necrodes surinamensis is nocturnal and highly attracted to artificial lights causing Ratcliffe(1996) to state concern for this species in cities where increased nocturnal lighting iscommon This may be the reason for the decrease or even the extirpation of this species atthis site As forNecrophilus pettiti it is a flightless carrion beetle species (Peck 1981) possiblylimiting its dispersal and survivability in increasingly urbanized areas Alternatively ouruse of hanging traps rather than pitfall traps as in Pirone amp Sullivan (1980)may explain theabsence of this flightless species in our study

In their study Gibbs amp Stanton (2001) discuss several ecological factors that mayinfluence the presence and relative abundance of carrion beetles in urban areas The firstlimiting factor is the availability of carcasses However urbanization can lead to an increasein abundance of some birds and small mammals (Faeth Bang amp Saari 2011 Pickett et al2011) Forests in New York City typically contain large rodent populations (particularlywhite-footed mice and chipmunks) as well as abundant songbird populations (Ekernas ampMertes 2006 Seewagen amp Slayton 2008) Availability of bird and small mammal carcassesin urban parks may be higher than previously appreciated and may explain the abundanceof some generalist species (Ni tomentosus) in NYC

Competition with scavengers may also limit carrion beetle abundance and diversityCompetitors for carrion include other invertebrates (flies and mitesmdashGibbs amp Stanton2001) and many vertebrate mesopredators that are abundant in cities (raccoons opossumscoyotes skunksmdashDeVault et al 2011) However Sugiura et al (2013) recently reportedthat resource competition between invertebrates and vertebrates for carrion was lessprevalent than previously thought Vertebrate competitors are likely present at all of ourstudy sites but may not substantially influence carrion beetle abundance particularly if theyare utilizing food resources provided by humans in cities As for intraspecific competitionwith other carrion beetle species Scott (1998) found there to be competition between Niorbicollis and Ni defodiens based on temperature Trumbo amp Bloch (2002) found that Nidefodiens can locate carcasses sooner than other species butNi orbicollis uses cues fromNidefodiens to locate and subsequently dominate carrion We identified a higher abundanceof Ni orbicollis than Ni defodiens especially in urban and suburban sites (Fig 2) Greaterabundance ofNi orbicollis in our sites could be due to these competitive abilities that aidNiorbicollis in locating and dominating prey more effectively Lastly intraspecific invertebratecompetitors such as flies are often very prevalent in human altered landscapes (Kavazos ampWallman 2012) Flies are known to quickly locate carcasses andmay outcompete beetles oncarrion (Scott 1998 Scott amp Traniello 1990 Trumbo 1990 Gibbs amp Stanton 2001) If thereis high fly abundance in NYC parks our study indicates that this intraspecific competitionis not restricting beetle abundance in urban forests compared to suburban and rural forestsSome carrion beetles have also evolved adaptations to thwart fly competition For exampleNi tomentosus was the most abundant carrion beetle in urban forests in this study andmay be thriving partially due to its cooperative burying behavior that rapidly concealscarcasses from flies during times of day when flies are most active (Scott Traniello ampFetherston 1987)

Gibbs amp Stanton (2001) also identify soil compaction as a negative influence on carrionbeetles in urban areas Soil compaction is characteristic of urban forests due to trampling by


humans and other factors and may impede the ability of beetles to dig and bury carcassesin urban soils (Gibbs amp Stanton 2001 Pouyat et al 2007) The relatively shallow buryingof Ni tomentosusmay be another factor promoting the success of this species in NYC (Fig2) In the study by Wolf amp Gibbs (2004) they found soil compaction to not be correlatedwith urbanized land but was partially correlated with forest extent Additionally largerforest area has been shown to support greater diversity of burying beetles (Gibbs amp Stanton2001) NYCrsquos urban parks seem to contain sufficiently extensive tracts of forest for carrionbeetles to persist despite possible soil compaction

We found no trend in body size (as classified via Scott 1998 Gibbs amp Stanton 2001)across habitat specialization (from Gibbs amp Stanton 2001) or with continuous foresthabitat area compared to abundance of species found in urban suburban and ruralsites Our results of body size and habitat specialization were again contradictory to pastburying beetle literature where Ulrich Komosiński amp Zalewski (2008) found a negativeassociation between body size of necrophagous beetles and distance from the city centerin northern Poland Gibbs amp Stanton (2001) also reported that carrion beetles thrivingin urban areas were often small-bodied and habitat generalists Magura Toacutethmeacutereacutesz ampLoumlvei (2006) used even more stringent statistical measures to assess carabid beetle bodysize across an urbanization gradient These studies measured body length andor biomassof each individual whereas our study was limited by gross approximation of body sizeclasses which may have caused us to miss this effect In a broader analysis of 69 beetlespecies (Davies amp Margules 2000) body size was not correlated with fragmentation Theauthors argued that the relationship between extinction risk and body size is very complexand influenced by other factors like spatial scale population fluctuation and longevity

In general our study shows that within NYC urban parks are able to house nearlythe same community as continuous forest tracts in the rural surrounding areas despitelocal impervious surface and ecologicallife history variability across species These resultshighlight the importance of maintaining and conserving large areas of forest throughoutNYC within city parks commonly used for human recreation

CONCLUSIONSUrban parks have the potential to house diverse habitats rich in biodiversity (Kotze et al2011) of both plants and animals (Angold et al 2006) Even highly modified landscapescontaining small reserves comprising ample green space have the potential to house largebeetle diversity (Watts amp Lariviere 2004) and high abundance of other arthropod species(Bolger et al 2008 Faeth Bang amp Saari 2011) The maintenance of arthropod biodiversityin urban parks may ultimately be mediated by human influence on plant communities(Faeth Bang amp Saari 2011) Alternatively arthropod species thriving in urban habitatsmaybe preadapted for tolerance to fragmentation and high colonization potential (Sattler et al2010) A current review on biodiversity in cities suggests that patch area and corridors havethe strongest positive effect on biodiversity and that we need to maintain sites with largerthan 50 hectares to prevent rapid loss of sensitive species (Beninde Veith amp Hochkirch2015) Maintenance of carrion beetle diversity in NYC will stabilize the interconnectedness


of urban food webs aid in nutrient cycling and promote natural decomposition ofcarcasses (Beasley Olson amp Devault 2015) in our urban parks Sustaining the ecosystemservices provided by carrion beetles will require conservation of large continuous foresttracts in urban parks Greater connectivity between small green areas and connectivitybetween the urban core and surrounding forested areas will promote the biodiversitypotential of small patches (Do amp Joo 2013) A lsquolsquoland sparing cityrsquorsquo approach is one way tomaintain essential ecosystem services (Stott et al 2015) provided by carrion beetles in theNew York City area

ACKNOWLEDGEMENTSWe thank Matthew Combs and Jane Park for photographing carrion beetles and ElizabethCarlen Carol Henger and Emily Puckett for helpful comments on the manuscriptGabor Lovei and two anonymous reviewers also provided very thorough and constructivesuggestions for improving the manuscripts

ADDITIONAL INFORMATION AND DECLARATIONS

FundingA Zhaorsquos work on this project was supported in part by a National Science FoundationREU Site grant (No 1063076) to Fordham University and the Louis Calder Center Noadditional external funding was received for this study The funders had no role in studydesign data collection and analysis decision to publish or preparation of the manuscript

Grant DisclosuresThe following grant information was disclosed by the authorsNational Science Foundation REU Site 1063076Fordham University and the Louis Calder Center

Competing InterestsThe authors declare there are no competing interests

Author Contributionsbull Nicole A Fusco and Anthony Zhao conceived and designed the experiments performedthe experiments analyzed the data wrote the paper prepared figures andor tablesreviewed drafts of the paperbull Jason Munshi-South conceived and designed the experiments performed theexperiments contributed reagentsmaterialsanalysis tools wrote the paper revieweddrafts of the paper

Field Study PermissionsThe following information was supplied relating to field study approvals (ie approvingbody and any reference numbers)

Permission to collect carrion beetles was granted by the New York City Department ofParks and Recreation the Rockefeller State Park Preserve and the Connecticut Departmentof Energy and Environmental Protection (Permit No 1214008)


Data AvailabilityThe following information was supplied regarding data availability

The raw data has been supplied as a Supplementary File

Supplemental InformationSupplemental information for this article can be found online at httpdxdoiorg107717peerj3088supplemental-information

REFERENCESAngold PG Sadler JP Hill MO Pullin A Rushton S Austin K Small E Wood B

Wadsworth R Sanderson R Thompson K 2006 Biodiversity in urban habitatpatches Science of the Total Environment 360196ndash204DOI 101016jscitotenv200508035

AronsonMFJ Sorte FA Nilon CH Katti M GoddardMA Lepczyk CAWarren PSWilliams NSG Cilliers S Clarkson B Dobbs C Dolan R HedblomM Klotz SKooijmans JL Kuhn I MacGregor-Fors I McDonnell M Mortberg U Pysek PSiebert S Sushinsky J Werner PWinter M 2014 A global analysis of the impactsof urbanization on bird and plant diversity reveals key anthropogenic driversProceedings of the Royal Society B Biological Sciences 28120133330DOI 101098rspb20133330

Baselga A Orme CDL 2012 Betapart an R package for the study of beta diversityMethods in Ecology amp Evolution 3808ndash812 DOI 101111j2041-210X201200224x

Beasley JC Olson ZH Devault TL 2015 Ecological role of vertebrate scavengers InUSDA National Wildlife Research Center Staff Publications Boca Raton CRC Press107ndash127

Beninde J VeithM Hochkirch A 2015 Biodiversity in cities needs space a meta-analysis of factors determining intra-urban biodiversity variation Ecological Letters18581ndash592 DOI 101111ele12427

Bolger DT Beard KH Suarez AV Case TJ 2008 Increased abundance of native and nonnative spiders with habitat fragmentation Diversity and Distributions 14655ndash665DOI 101111j1472-4642200800470x

Buttigieg PL Ramette A 2014 A guide to statistical analysis in microbial ecology acommunity-focused living review of multivariate data analyses FEMS MicrobialEcology 90543ndash550 DOI 1011111574-694112437

Davies KF Margules C 2000Which traits of species predict population declines inexperimental forest fragments Ecology 811450ndash1461DOI 1018900012-9658(2000)081[1450WTOSPP]20CO2

Deichsel R 2006 Species change in an urban setting-ground and rove beetles(Coleoptera Carabidae and Staphylinidae) in Berlin Urban Ecosystems 9161ndash178DOI 101007s11252-006-8588-3

DeVault TL Olson ZH Beasley JC Rhodes OE 2011Mesopredators dominatecompetition for carrion in an agricultural landscape Basic and Applied Ecology12268ndash274 DOI 101016jbaae201102008


Diamond SE Dunn RR Frank SD Haddad NMMartin RA 2015 Shared and uniqueresponses of insects to the interaction of urbanization and background climateCurrent Opinion in Insect Science 1171ndash77 DOI 101016jcois201510001

Didham RK 2010 Ecological consequences of habitat fragmentation In Encyclopedia oflife sciences Chichester John Wiley amp Sons Ltd

Do Y Joo GJ 2013 The effect of fragmentation and intensive management on carabidbeetles in coniferous forest Applied Ecology and Environmental Research 11451ndash461DOI 1015666aeer1103_451461

Ekernas SL Mertes KJ 2006 The influence of urbanization patch size and habitat typeon small mammal communities in the New York metropolitan region New YorkWildMetro

Elek Z Loumlvei GL 2007 Patterns in ground beetle (Coleoptera Carabidae) assemblagesalong an urbanization gradient in Denmark Acta Oecologica 32104ndash111DOI 101016jactao200703008

Elmqvist T Fragkias M Goodness J Guumlneralp B Marcotullio PJ McDonald RIParnell S Schewenius M SendstadM Seto KCWilkinson C 2013Urbanizationbiodiversity and ecosystem services challenges and opportunities a global assessmentSpringer

ESRI (Environmental Systems Resource Institute) 2014 ArcMap 103 Redlands ESRIFaeth SH Bang C Saari S 2011 Urban biodiversity patterns and mechanisms Annals of

the New York Academy of Sciences 122369ndash81 DOI 101111j1749-6632201005925xGaublomme E Hendrickx F Dhuyvetter H Desender K 2008 The effects of forest

patch size and matrix type on changes in carabid beetle assemblages in an urbanizedlandscape Biological Conservation 1412585ndash2596 DOI 101016jbiocon200807022

Gibbs JP Stanton EJ 2001Habitat fragmentation and arthropod community changecarrion beetles phoretic mites and flies Ecological Applications 11(1)79ndash85

GrimmNB Faeth SH Golubiewski NE Redman CLWu J Bai X Briggs JM2008 Global change and the ecology of cities Science 319(5864)756ndash760DOI 101126science1150195

Hamer AJ Parris KM 2011 Local and landscape determinants of amphibian communi-tiesin urban ponds Ecological Applications 21378ndash390 DOI 10189010-03901

Hanley GA Cuthrell DL 2008 Carrion beetles of North Dakota including speciesdescriptions and identification keys for the entire North American Silphid faunaCyril Moore Science Center Science Monograph 41ndash52

Homer CG Dewitz JA Yang L Jin S Danielson P Xian G Coulston J Herold NDWickham JD Megown K 2011 2011 National land cover database for the conter-minous United States-representing a decade of land cover change information Pho-togrammetric Engineering and Remote Sensing 81(5)345ndash354 DOI 1023071938106

Hornung EB Tothmeresz T Magura T Vilisics F 2007 Changes of isopod assemblagesalong an urban-suburban-rural gradient in Hungary European Journal of Soil Biology43158ndash165 DOI 101016jejsobi200701001


Jaccard P 1901 Distribution de la flore alpine dans le bassin des Dranses et dansquelques reacutegions voisines Bulletin de la Socieacuteteacute Vaudoise des Sciences Naturelles37241ndash272

Jost L 2006 Entropy and diversity Oikos 113363ndash375DOI 101111j20060030-129914714x

Kavazos CRJ Wallman JF 2012 Community composition of carrion-breeding blowflies(Diptera Calliphoridae) along an urban gradient in south-eastern Australia Land-scape and Urban Planning 106183ndash190 DOI 101016jlandurbplan201203002

Klein BC 1989 Effects of forest fragmentation on dung and carrion beetle communitiesin central Amazonia Ecology 701715ndash1725

Kotze J Venn S Niemelauml J Spence J 2011 Effects of urbanization on the ecology andevolution of arthropods In Urban Ecological Patterns Processes amp ApplicationsOxford Oxford University Press 159ndash166

La Sorte FA AronsonMFJ Williams NSG Celesti-Grapow L Cilliers S 2014 Betadi-versity of urban floras among European and non-European cities Global Ecology andBiogeography 23769ndash779 DOI 101111geb12159

Lessard JP Buddle CM 2005 The effects of urbanization on ant assemblages (Hy-menoptera Formicidae) associated with the Molson Nature Reserve Quebec TheCanadian Entomologist 137215ndash225 DOI 104039n04-055

Magura T Lovei GL Tothmeresz B 2010 Does urbanization decrease diversity inground beetle (Carabidae) assemblages Global Ecology Biogeography 1916ndash26DOI 101111j1466-8238200900499x

Magura T Nagy D Tothmeresz B 2013 Rove beetles respond heterogeneously tourbanization Journal of Insect Conservation 17715ndash724DOI 101007s10841-013-9555-y

Magura T Toacutethmeacutereacutesz B Loumlvei GL 2006 Body size inequality of carabids along anurbanisation gradient Basic amp Applied Ecology 7472ndash482DOI 101016jbaae200508005

Martinson HM RauppMJ 2013 A meta-analysis of the effects of urbanization onground beetle communities Ecosphere 4(5)1ndash24 DOI 101890ES12-002621

McDonnell MJ Hahs AK 2008 The use of gradient analysis studies in advancing ourunderstanding of the ecology of urbanizing landscapes current status and futuredirections Landscape Ecology 231143ndash1155 DOI 101007s10980-008-9253-4

McKinneyML 2008 Effects of urbanization on species richness a review of plants andanimals Urban Ecosystems 11161ndash176 DOI 101007s11252-007-0045-4

Munshi-South J Kharchenko K 2010 Rapid pervasive genetic differentiation of urbanwhite-footed mouse (Peromyscus leucopus) populations in New York CityMolecularEcology 194242ndash4254

Munshi-South J Zolnik CP Harris SE 2016 Population genomics of the anthropoceneurbanization reduces the evolutionary potential of small mammal populationsEvolutionary Applications 9(4)546ndash564 DOI 101111eva12357


Niemelauml J Kotze DJ 2009 Carabid beetle assemblages along urban to rural gradients areview Landscape amp Urban Planning 9265ndash71DOI 101016jlandurbplan200905016

New York City Department of City Planning 2002 Land use facts 27 May 2002 NewYork New York City Department of City Planning Available at http archiveisX4usQselection-11410-114122

Oksanen J Blanchet FG Kindt R Legendre P Minchin PR OrsquoHara RB Simpson GLSolymos P Stevens MHHWagner H 2016 Vegan community ecology package Rpackage version 23-4 Available at httpsCRANR-projectorgpackage=vegan

OrdentildeanaM Crooks KR Boydston EE Fisher RN Lyren LM Siudyla S Haas CDHarris S Hathaway SA Turschak GMMiles AK Van Vuren DH 2010 Effects ofurbanization on carnivore species distribution and richness Journal of Mammalogy911322ndash1331 DOI 10164409-MAMM-A-3121

Peck SB 1981 Distribution and biology of flightless carrion beetle Necrophilus pettiti ineastern North America (Coleoptera Silphidae) Entomological News 92(5)181ndash185

Pickett STA CadenassoML Grove JM Boone CG Groffman PM Irwin E KaushalSS Marshall V McGrath BP Nilon CH Pouyat RV Szlavecz K Troy AWarrenP 2011 Urban ecological systems scientific foundations and a decade of progressJournal of Environmental Management 92331ndash362DOI 101016jjenvman201008022

Pirone DJ Sullivan DJ 1980 Ecology of necrophilous and carpophilous coleopterain a southern New York woodland (phenology aspection trophic and habitatpreferences) New York Entomological Society LXXXVIII(3)186ndash196

Pouyat RV Yesilonis ID Russell-Anelli J Neerchal NK 2007 Soil chemical andphysical properties that differentiate urban land-use and cover types Soil ScienceSociety of America Journal 71(3)1010ndash1019 DOI 102136sssaj20060164

R Core Team 2015 R a language and environment for statistical computing Vienna RFoundation for Statistical Computing Available at httpwwwR-projectorg

Ratcliffe BC 1996 The carrion beetles (Coleoptera Silphidae) of Nebraska Bulletin ofthe University of Nebraska State Museum 1343ndash54

Sattler T Duelli P Obrist MK Arlettaz R Moretti M 2010 Response of arthropodspecies richness and functional groups to urban habitat structure and managementLandscape Ecology 25941ndash954 DOI 101007s10980-010-9473-2

Saunders DA Hobbs RJ Margules CR 1991 Biological consequences of ecosystem frag-mentation a review Conservation Biology 518ndash32DOI 101111j1523-17391991tb00384x

Savage AM Hackett B Gueacutenard B Youngsteadt EK Dunn RR 2015 Fine-scaleheterogeneity across Manhattanrsquos urban habitat mosaic is associated with variationin ant composition and richness Insect Conservation and Diversity 8216ndash228DOI 101111icad12098

Scott MP Traniello JFA 1990 Behavioral and ecological correlates of male and femaleparental and reproductive success in the burying beetle Nicrophorus orbicollisAnimal Behavior 39274ndash283 DOI 101016S0003-3472(05)80871-1


Scott MP 1998 The ecology and behavior of burying beetles Annual Reviews of Entomol-ogy 43595ndash618 DOI 101146annurevento431595

Scott MP Traniello JFA Fetherston IA 1987 Competition for prey between ants andburying beetles (Nicrophorus Spp) differences between northern and southern tem-perate sites Psyche a Journal of Entomology 94325ndash332 DOI 101155198756594

Seewagen CL Slayton EJ 2008Mass changes of migratory land birds during stopoversin a New York City Park The Wilson Journal of Ornithology 120(2)296ndash303DOI 10167607-0871

Simpson EH 1949Measurement of diversity Nature 163688 DOI 101038163688a0Stott I SogaM Inger R Gaston KJ 2015 Land sparing is crucial for urban ecosystem

services Frontiers in Ecology and the Environment 13387ndash393 DOI 101890140286Sugiura S Tanaka R Taki H Kanzaki N 2013 Differential responses of scavenging

arthropods and vertebrates to forest loss maintain ecosystem function in a hetero-geneous landscape Biological Conservation 159206ndash213DOI 101016jbiocon201211003

Trumbo ST 1990 Reproductive success phenology and biogeography of burying beetles(Silphidae Nicrophorus) the American Midland Naturalist Vol 124 Notre Dam TheUniversity of Notre Dame 1ndash11

Trumbo ST Bloch PL 2000Habitat fragmentation and burying beetle abundanceJournal of Insect Conservation 4245ndash252 DOI 101023A1011390215088

Trumbo S Bloch PL 2002 Competition between Nicrophorus orbicollis and Nicrophorusdefodiens resource locating efficiency and temporal partitioning NortheasternNaturalist 913ndash26

UlrichW Komosiński K Zalewski M 2008 Body size and biomass distributions ofcarrionvisiting beetles do cities host smaller species Ecological Resources 23241ndash248DOI 101007s11284-007-0369-9

United Nations Department of Economic and Social Affairs Population Division2014World urbanization prospects the 2014 revision highlights (STESASERA352)

United States Census Bureau 2010 lsquolsquoDecennial Census 2010rsquorsquo Census US Departmentof Commerce Available at httpwwwcensusgovquickfacts tablePST04521536119(accessed on 29 February 2016)

Varet M Peacutetillon J Burel F 2011 Comparative responses of spider and carabid beetleassemblages along an urban-rural boundary gradient Journal of Arachnology39236ndash243 DOI 101636CP10-821

Watts C Lariviere M 2004 The importance of urban reserves for conserving beetlecommunities a case study from New Zealand Journal of Insect Conservation 47ndash58

Wolf JM Gibbs JP 2004 Silphids in urban forests diversity and function UrbanEcosystems 7371ndash384 DOI 101007s11252-005-6836-6

Xian G Homer C Demitz J Fry J Hossain NWickham J 2011 Change of impervioussurface area between 2001 and 2006 in the conterminous United States Photogram-metric Engineering and Remote Sensing 77758ndash762


use with natural habitats typically occurring only in small fragmented patches (SaundersHobbs amp Margules 1991) Fragmentation in cities often decreases species richness changescommunity composition and alters ecosystem processes (Didham 2010) Many speciesare impacted negatively by urbanization (carnivoresmdashOrdentildeana et al 2010 arthropodsmdashSattler et al 2010 amphibiansmdashHamer amp Parris 2011 birds amp plantsmdashAronson et al2014) but effects vary based on the taxonomic group in question (McKinney 2008) Forexample studies of arthropod diversity along urban-to-rural gradients have documenteda wide variety of responses to urbanization (Hornung et al 2007 Niemelauml amp Kotze2009 Varet Peacutetillon amp Burel 2011 Magura Nagy amp Tothmeresz 2013 Savage et al 2015Diamond et al 2015) Given the extreme variety of life history traits and habitat use amongarthropods responses to urbanization may be difficult to predict

Carrion beetles use small mammal carcasses as food sources for their young (Scott 1998)These beetles bury carcasses to avoid competition with other scavengers thus facilitatingdecomposition and providing considerable ecosystem services Availability of carrionlikely influences the abundance and diversity of carrion beetles Carrion beetle speciescompete with each other as well as with other scavenging vertebrates (Scott 1998 Trumboamp Bloch 2000 DeVault et al 2011) and invertebrates for this resource (Ratcliffe 1996Gibbs amp Stanton 2001) Urbanization alters natural habitats in myriad ways (Grimm et al2008) that may cause local extirpations or reduced abundance of native small mammals(eg likely carrion) and carrion beetles in cities

Gibbs amp Stanton (2001) previously reported that forest fragmentation reduced carrionbeetle species richness and abundance in Syracuse New York Beetles that persisted in thesefragments were primarily small-bodied habitat generalists and other carrion beetles mayhave declined in abundance due to lower carcass availability increased prevalence of otherscavengers or reduced soil and litter quality Wolf amp Gibbs (2004) also found that forestfragmentation decreased carrion beetle diversity and abundance in Baltimore MarylandThey argued that forest contiguity was an important factor affecting richness abundanceand diversity of carrion beetles in this city However these studies did not directly addresswhether large parks within core urban areas harbor a substantial diversity of carrion beetles

In this study we investigated species richness diversity relative abundance and com-munity similarity of carrion beetles (Family Silphidae) across an urban-to-rural gradientin the New York City (NYC) metropolitan area NYC is the most densely populated areain North America but 27 of the cityrsquos land area is comprised of vegetated natural areasparticularly within several large urban parks (New York City Department of City Planning2002) These parks are characterized by substantial forest cover and high densities of smallmammals (Munshi-South amp Kharchenko 2010) and thus may provide high-quality habitatfor a diverse assemblage of carrion beetles Alternatively NYCrsquos urban forests may harborless carrion beetle diversity relative to suburban and rural areas outside of NYC as wasfound in Baltimore and Syracuse (Gibbs amp Stanton 2001 Wolf amp Gibbs 2004) We alsocompared historical records from a single site (Pirone amp Sullivan 1980) the Louis CalderCenter in Armonk New York with our 2015 estimates of carrion beetle diversity andabundance to examine changes over the last four decades The forest area at the LouisCalder Center has not changed in that time but urbanization of the surrounding area and














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Necrophilaamericana


LCC1 8 54 0 0 0 0 28 9LCC2 26 168 0 1 0 0 7 25LCC3 5 35 0 2 0 0 20 7






0

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50

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100

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orb

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Ni

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bo

race

nse

Ne a

me

rica

na

Species

Re

lativ

e A

bu

nd

an

ce

(

)

Site Classification

Urban

Suburban

Rural




= 0028 pgt




Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species





Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Ne

pet

titi

Ne

sur

anam

ensi

s

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species

LCC 1974LCC 2015






minus05 00 05

minus06

minus04

minus02

00

02

04

NMDS1

NMDS2

CP

CFP

SWP

CATCT

NYBG

RSP

LCC

IHP

MRG

VCP

HBPCSH





MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)



















































































































CCJ= SJ= a(a+b+ c)













Nicrophorussayi

Oiceoptomainaequale


Necrophilaamericana


LCC1 8 54 0 0 0 0 28 9LCC2 26 168 0 1 0 0 7 25LCC3 5 35 0 2 0 0 20 7






0

25

50

75

100

Ni

orb

ico

llis

Ni

tom

en

tosu

s

Ni

de

fod

ien

s

Ni

pu

stu

latu

s

Ni

sayi

O in

eq

ua

le

O n

ove

bo

race

nse

Ne a

me

rica

na

Species

Re

lativ

e A

bu

nd

an

ce

(

)

Site Classification

Urban

Suburban

Rural




= 0028 pgt




Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species





Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Ne

pet

titi

Ne

sur

anam

ensi

s

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species

LCC 1974LCC 2015






minus05 00 05

minus06

minus04

minus02

00

02

04

NMDS1

NMDS2

CP

CFP

SWP

CATCT

NYBG

RSP

LCC

IHP

MRG

VCP

HBPCSH





MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)

























































































































Nicrophorussayi

Oiceoptomainaequale


Necrophilaamericana


LCC1 8 54 0 0 0 0 28 9LCC2 26 168 0 1 0 0 7 25LCC3 5 35 0 2 0 0 20 7






0

25

50

75

100

Ni

orb

ico

llis

Ni

tom

en

tosu

s

Ni

de

fod

ien

s

Ni

pu

stu

latu

s

Ni

sayi

O in

eq

ua

le

O n

ove

bo

race

nse

Ne a

me

rica

na

Species

Re

lativ

e A

bu

nd

an

ce

(

)

Site Classification

Urban

Suburban

Rural




= 0028 pgt




Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species





Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Ne

pet

titi

Ne

sur

anam

ensi

s

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species

LCC 1974LCC 2015






minus05 00 05

minus06

minus04

minus02

00

02

04

NMDS1

NMDS2

CP

CFP

SWP

CATCT

NYBG

RSP

LCC

IHP

MRG

VCP

HBPCSH





MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)















































































































0

25

50

75

100

Ni

orb

ico

llis

Ni

tom

en

tosu

s

Ni

de

fod

ien

s

Ni

pu

stu

latu

s

Ni

sayi

O in

eq

ua

le

O n

ove

bo

race

nse

Ne a

me

rica

na

Species

Re

lativ

e A

bu

nd

an

ce

(

)

Site Classification

Urban

Suburban

Rural




= 0028 pgt




Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species





Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Ne

pet

titi

Ne

sur

anam

ensi

s

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species

LCC 1974LCC 2015






minus05 00 05

minus06

minus04

minus02

00

02

04

NMDS1

NMDS2

CP

CFP

SWP

CATCT

NYBG

RSP

LCC

IHP

MRG

VCP

HBPCSH





MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)















































































































Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species





Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Ne

pet

titi

Ne

sur

anam

ensi

s

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species

LCC 1974LCC 2015






minus05 00 05

minus06

minus04

minus02

00

02

04

NMDS1

NMDS2

CP

CFP

SWP

CATCT

NYBG

RSP

LCC

IHP

MRG

VCP

HBPCSH





MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)















































































































Ni

orbi

colli

s

Ni

tom

ento

sus

Ni

defo

dien

s

Ni

pust

ulat

us

Ni

sayi

O n

oveb

orac

ense

O i

nequ

ale

Ne

am

eric

ana

Ne

pet

titi

Ne

sur

anam

ensi

s

Re

lativ

e A

bu

nd

an

ce

(

)

0

20

40

60

80

100

Species

LCC 1974LCC 2015






minus05 00 05

minus06

minus04

minus02

00

02

04

NMDS1

NMDS2

CP

CFP

SWP

CATCT

NYBG

RSP

LCC

IHP

MRG

VCP

HBPCSH





MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)















































































































minus05 00 05

minus06

minus04

minus02

00

02

04

NMDS1

NMDS2

CP

CFP

SWP

CATCT

NYBG

RSP

LCC

IHP

MRG

VCP

HBPCSH





MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)















































































































MRG

SWP

VCP

NYBG

CP

IHP

HBP

CAT

CFP

CSH

LCC

RSP

CT000

005

010

015

020

025

Height

βjtu

HBP

CAT

CFP

IHP

NYBG

CT

LCC

RSP

CSH

VCP

SWP

CP

MRG

00

01

02

03

04

05

Height

βjne

(A)

(B)















































































































urban forests sustain diverse carrion beetle …urban forests sustain diverse carrion beetle...

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