Myctophid feeding ecology and carbon transport along the northernMid-Atlantic Ridge

Jeanna M. Hudson a,n, Deborah K. Steinberg a,nn, Tracey T. Sutton b,John E. Graves a, Robert J. Latour a

a Virginia Institute of Marine Science, College of William & Mary, P.O. Box 1346, Gloucester Point, VA 23062, USAb NSU Oceanographic Center, 8000 North Ocean Drive, Dania Beach, FL 33004, USA

a r t i c l e i n f o

Article history:Received 25 April 2014Received in revised form4 July 2014Accepted 8 July 2014Available online 24 July 2014

Keywords:LanternfishDietZooplanktonMesopelagicDiel vertical migrationBiological pump

a b s t r a c t

Myctophids are among the most abundant fishes in the world's ocean and occupy a key position inmarine pelagic food webs. Through their significant diel vertical migrations and metabolism they alsohave the potential to be a significant contributor to carbon export. We investigated the feeding ecologyand contribution to organic carbon export by three myctophid species, Benthosema glaciale, Proto-myctophum arcticum, and Hygophum hygomii, from a structurally and ecologically unique ecosystem- theMid-Atlantic Ridge (MAR). Similar to the results of previous studies, the diet of these fishes wasprimarily copepods and euphausiids, however, gelatinous zooplankton was identified in the diet ofB. glaciale for the first time. Ridge section and time of day were significant explanatory variables in thediet of B. glaciale as determined by canonical correspondence analysis, while depth was the onlysignificant explanatory variable in the diet of P. arcticum. Daily consumption by MAR myctophids wasless than 1% of dry body weight per day and resulted in the removal of less than 1% of zooplanktonbiomass daily. Although lower than previous estimates of carbon transport by myctophids andzooplankton in other areas, MAR myctophid active transport by diel vertical migration was equivalentto up to 8% of sinking particulate organic carbon in the North Atlantic. While highly abundant,myctophids do not impart significant predation pressure on MAR zooplankton, and play a modest rolein the active transport of carbon from surface waters.

& 2014 Elsevier Ltd. All rights reserved.

1. Introduction

Fishes of the family Myctophidae are an important componentof the marine pelagic food web due to their abundance and dualityas both prey and predator in the epi- and mesopelagic zones.Myctophids are important prey for deep-sea and epipelagicpiscivorous fishes, marine mammals, and sea birds (Hopkins et al.,1996; Beamish et al., 1999; Pusineri et al., 2008; Pereira et al.,2011). As predators, myctophids feed primarily on crustaceanzooplankton, but are also known to feed on gelatinous zooplank-ton, pteropods, and other non-crustacean prey including fishes(Kinzer, 1982; Sameoto, 1988; Hopkins et al., 1996; Moku et al.,2000). Within midwater fish assemblages, myctophids can be themost important consumer (Hopkins et al., 1996), and have asignificant impact on zooplankton populations, consuming 8–16%of the total copepod daily production and 2% of the overallzooplankton biomass each night in the Gulf of Mexico (Hopkins

and Gartner, 1992), and 2–31% of the zooplankton standing stockdaily in the equatorial Pacific (Gorelova, 1984).

In this study, we focus on the feeding ecology of myctophidsfrom a structurally and ecologically unique ecosystem – the Mid-Atlantic Ridge (MAR). The MAR was the location of a project todescribe and understand the patterns of distribution, abundance,and trophic relationships of organisms inhabiting the northernMAR between Iceland and the Azores (MAR-ECO; Bergstad, 2002).Sutton et al. (2008) characterized the midwater fish compositionat the MAR during June–July, 2004 and reported that the familyMyctophidae was the numerically dominant fish family (59% of allfishes collected), with one species, Benthosema glaciale, the mostabundant species collected.

Diet studies of myctophids from seamounts (Pusch et al., 2004,Colaço et al., 2013) show elevated feeding, which is hypothesized tobe due to turbulent mixing resulting from the unique hydrographyassociated with these structures (Pusch et al., 2004). Structurallysimilar to seamounts, mid-ocean ridges have the potential to increasefood availability to benthic and planktonic consumers throughresuspension of sediment (Genin and Boehlert, 1985; Dower et al.,1992; Muriño et al., 2001) and trapping of laterally advected andvertically migrating zooplankton by the raised bottom of the ridge

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Deep-Sea Research I

http://dx.doi.org/10.1016/j.dsr.2014.07.0020967-0637/& 2014 Elsevier Ltd. All rights reserved.

n Corresponding author. Tel.: þ1 804 684 7165.nn Corresponding author. Tel.: þ1 804 684 7838.E-mail addresses: jeannak@vims.edu (J.M. Hudson),

debbies@vims.edu (D.K. Steinberg).

Deep-Sea Research I 93 (2014) 104–116

(Genin and Dower, 2007; Porteiro and Sutton, 2007), which maysustain a unique community and trophic structure compared to off-ridge waters. Although several studies have reported on the feedingecology of myctophid species from seamounts or other environments(Hopkins et al., 1996; Pakhomov et al., 1996; Pusch et al., 2004;Petursdottir et al., 2008; Dypvik et al., 2012), none exist formyctophids from mid-ocean ridge systems.

Furthermore, little quantitative data exist on the role of theseabundant consumers in carbon cycling. Many myctophid speciesmake daily vertical migrations to the epipelagic zone at night tofeed on zooplankton, and migrate to deeper water (�400–1000 m) during the day where apparently most of the food isdigested (Baird et al., 1975). By metabolizing this surface-derivedfood in the mesopelagic zone, myctophids actively transportorganic and inorganic carbon to depth, a process which is animportant component of the biological pump (Ducklow et al.,2001). Active transport of carbon via mortality, egestion of fecalpellets, respiration of CO2, and excretion of dissolved organiccarbon at depth have been determined for vertically migratingzooplankton in a variety of environments (e.g., Longhurst et al.,1990; Steinberg et al., 2000; Al-Mutairi and Landry, 2001), butonly two previous studies have quantified active transport byvertically migrating myctophids. Hidaka et al. (2001) reportedmyctophids in the equatorial Pacific actively transported theequivalent of 15–28% of passively sinking particulate organiccarbon (POC) measured by sediment traps, and Davison et al.(2013) estimated myctophid vertical migration could account for�8% of passively sinking POC (as estimated from satellite data) inthe northeast Pacific Ocean. There are no previous estimates ofactive transport by myctophids for the Atlantic Ocean.

The first goal of our study was to describe and quantify thefeeding ecology of three myctophid species from the northernMAR (Benthosema glaciale, Protomyctophum arcticum, and Hygo-phum hygomii) to investigate how the presence of a mid-oceanridge may affect myctophid diet composition. Our second goal wasto provide an estimate of active carbon transport by myctophids atthe MAR, a first for the North Atlantic Ocean. Diet composition,daily consumption rates, and carbon export of these fishes wereused to assess their role in the overall trophic structure andcarbon cycle of this topographically and hydrodynamically uniqueecosystem.

2. Methods

2.1. Sampling procedure

Myctophids were collected during the R/V G.O. Sars researchexpedition to the northern MAR (Iceland to the Azores) duringJune–July, 2004. Two double-warp, multi-cod end midwater trawlswere used to sample the ridge fauna in discrete depth zones. Themacrozooplankton trawl has a 6�6 m mouth opening, 6 mmstretched mesh throughout its length, and was equipped with fiveopening and closing cod ends. The Åkra trawl has a 20–35 mvertical mouth opening, 110 m door-spread, graded mesh to22 mm (stretched), and was equipped with three multiple openingand closing cod ends. Volume of water filtered was calculatedusing the trawl mouth area, towing speed, and distance traveled.

Predefined stations along the ridge were sampled discretelywithin five depth categories: 0–200, 200–750, 750–1500, 1500–2300, and 42300 m in four ridge sections (Fig. 1). Samples wereclassified as day (D), dusk (DN), night (N), or dawn (ND) with duskand dawn samples defined as the start time of the net being onehour before to one hour after sunset and sunrise, respectively(Sutton et al., 2008). Once on board, specimens were sorted andeither frozen whole or preserved in 10% buffered formalin.

Preserved samples were identified and transferred to 70% ethanolin the laboratory. For additional details concerning net samplingaboard the R/V G.O. Sars, (see Wenneck et al., 2008).

Trawl gear provides measures of relative fish biomass (Koslowet al.,1997; Kaartvedt et al., 2012), which implies information ongear efficiency is needed for the estimation of any biomass-normalized rate processes. Using hydroacoustics, Kaartvedt et al.(2012) reported a value of 0.14 for the sampling efficiency of B.glaciale collected by a large (�400 m2 mouth area) Harstad trawlnet. For the gears used in the present study, Heino et al. (2011)determined the Åkra trawl was more efficient at sampling fishesthan the macrozooplankton trawl, with a relative catchability of2.3. Despite the improved efficiency of the Åkra trawl, we electedto base our myctophid biomass and carbon transport calculationson data obtained by the macrozooplankton trawl since the fixedmouth area of this gear allowed for a more accurate calculation ofvolume of water filtered. For all calculations based on datacollected by the macrozooplankton trawl, both the actual biomassand biomass corrected for an assumed sampling efficiency of 0.14are reported.

2.2. Sample selection, dissection, and prey identification

Three myctophid species were selected for analysis – Bentho-sema glaciale, Protomyctophum arcticum, and Hygophum hygomii –based on their diverse geographic distributions and availability ofsamples. A subset of specimens from the total cruise catch wasselected for measurement and dissection from the availablegeographic-location, depth, and time-of-day combinations. A totalof 380 fishes were processed for diet composition informationbroken down by species as follows: 265 B. glaciale, 76 P. arcticum,and 39 H. hygomii. The standard length of each fish was recordedto the nearest 0.1 mm and the stomach and intestines wereexcised. Prey was identified microscopically to the lowest possible

Fig. 1. Trawl sampling stations at four ridge sections along the northern Mid-Atlantic Ridge from Iceland to the Azores during the 2004 R/V G.O. Sars MAR-ECOexpedition. Black line represents the approximate location of the Sub-polar Front(301W, 521N) at the time of the cruise.

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116 105

taxonomic level using a Nikon SMZ 1000 dissecting microscope.Diet descriptions and analyses included prey from stomachs only;intestinal prey were not included due to the tendency foradvanced digestion resulting in low taxonomic resolution. Preytypes that were observed infrequently were grouped using genusor family classifications to increase sample size. Diet indices werecalculated for the lowest taxonomic level of grouped prey typesthat provided adequate sample size, as well as for broad preycategories at the subclass level (e.g., copepods) (Table 1).

2.3. Prey measurements

The length and width of each prey item was recorded to thenearest 0.01 mm using Image Pro Plus 5.0 software. Cephalosomeand urosome length and width measurements were determinedfor copepods. Total length and width were determined for all preyfor which body measurements were possible. For well-digestedprey, average body measurements from intact, related taxa wereused, while hook length was used to determine body length andwidth of chaetognaths (Pearre 1980; Terazaki 1993). Body mea-surements of prey items were used to calculate body volume usingformulae for the most similar geometric shape. Prey volume wasthen used to estimate wet weight (assuming specific gravity-¼1.0 g cc�1). Crustacean dry weight was calculated as 20% of wetweight and carbon as 40% of dry weight (Silver and Gowing, 1991;Steinberg et al., 1998). Conversion factors for other, less abundant,prey taxa were utilized as described in Larson (1986) andSteinberg et al. (1998).

2.4. General diet description

The diet of each myctophid species was summarized usingthree diet indices: percent frequency of occurrence, percentcomposition by number, and percent dry weight (Hyslop, 1980).The indices, represented generally as %Ik, were calculated using acluster sampling estimator (Buckel et al., 1999; Latour et al., 2008)of the following form:

%Ik ¼∑n

i ¼ 1Miqik∑n

i ¼ 1Mi� 100 ð1Þ

such that

qik ¼wik

wið2Þ

where k represents prey type, n is the number of cod endscontaining a predator, and Mi is the number of predators collectedin cod end i (with one cod end representing one depth zone at anindividual station). In Eq. (2), qik represents the proportion ofoccurrence, abundance, or weight of each prey type in each codend. Diet composition indices were calculated as a weightedaverage of qik with the abundance of each predator, Mik, as theweighting factor. The variance for each diet index was calculatedas

varð%IkÞ ¼1

nM2

∑ni ¼ 1M

2i ðqik� IkÞ2

n�1� 1002 ð3Þ

after Latour et al. (2008), where M is the average number of aparticular predator collected in a cod end, and was used tocalculate standard error for each diet index.

2.5. Ontogenetic and spatial changes in diet

To examine spatial and ontogenetic patterns in the diet,individuals of B. glaciale and P. arcticum (there were too few H.hygomii to conduct these analyses) were grouped into narrow,5 mm size classes with the members of each class having a

relatively similar diet composition. The proportion of dry weightof each prey type was then calculated for each size class. Dryweight was used as the reference index to investigate dietarypatterns as it is the least biased compared to abundance andfrequency of occurrence indices which are heavily influenced bythe size and number of prey. The narrow size classes were groupedinto broader categories with similar prey composition based onprey weight using cluster analysis (Euclidean distance, averagelinkage method, Sokal and Michener, 1958). A scree plot was usedto determine the number of clusters based on the average distancebetween clusters.

Canonical correspondence analysis (CCA, ter Braak, 1986),a method which extracts the major gradients in a data set thatcan be accounted for by the measured explanatory variables(McGarigal et al., 2000), was used to investigate the relationshipbetween the diets of B. glaciale and P. arcticum and ridge section(RR, CGFZ, FSZ, AZ), depth zone (DZ 1, 0–200 m; DZ 2, 200–750 m;DZ 3, 750–1500 m), and time of day (day, dusk, night, dawn). Eachelement of the response matrix for the CCA was the mean percentdry weight of a given prey type in a particular depth, ridge section,and time-of-day combination. Variability is explained by thecanonical axes, which are linear combinations of the independentexplanatory variables. Significance of the explanatory variableswas determined using ANOVA, and a biplot was constructed toexplore the relationships between the explanatory variables andprey weight. The CCA and cluster analysis were performed usingR version 2.12.0.

2.6. Gastric evacuation and daily consumption

Daily consumption for myctophids in specific ridge sectionswas calculated using an evacuation rate model based on Elliott andPersson (1978). Consumption (Cdkr, μg DW d�1

fish�1) was calcu-lated as

Cdkr ¼ 24ErSkr ð4Þwhere 24 is the number of hours in a day, Er is the evacuation rate(h�1) at ridge section r, and Skr is the mean stomach content dryweight of predator k (μg DW prey fish�1) from ridge section r(Durbin et al., 1983; Link and Garrison, 2002; Tanaka et al., 2013).A temperature-based evacuation rate model was derived from aregression analysis of compiled myctophid gut evacuation rateinformation (E¼0.0942e0.0708t, where t represents temperature in1C, Table 2; Pakhomov et al., 1996). The bulk of digestion bymyctophids was assumed to occur within depth zone 2 (200–750 m) and day time temperature information collected synopti-cally with fish sampling in depth zone 2 was used to derive ridgesection-specific evacuation rates. Daily consumption rates per fishwere converted to consumption per unit of average myctophidbiomass and were multiplied by the biomass of all myctophidspecies combined. Myctophid biomass was integrated to 2300 mto provide a range of possible daily consumption estimates(μg DW m�2 d�1) of MAR myctophids.

2.7. Active carbon export by diel vertical migration

Active carbon export to below 200 m via myctophid respirationof CO2, excretion of dissolved organic carbon (DOC), and egestionof POC in the form of fecal pellets were calculated for ridgesections at which both day and night tows were performed indepth zone 1 (0–200 m) and for which night time myctophidbiomass was greater than day time myctophid biomass in depthzone 1. The RR and AZ were the only ridge sections at which thesecriteria were met, with two day and two night tows performed ateach ridge section. Migrator biomass was defined as the difference

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116106

Table 1Prey composition from stomachs of Benthosema glaciale, Protomyctophum arcticum, and Hygophum hygomii collected during a cruise to the Mid-Atlantic Ridge during June–July, 2004. n is sample size, %W is percent dry weight, %N is percent composition by number and %F is percent frequency of occurrence of each prey taxa. (�) indicates preywas absent.

Prey B. glaciale P. arcticum H. hygomii

n %W %N %F n %W %N %F n %W %N %F

CopepodaCalanoidaAetideus sp. 1 0.36 0.70 9.46 4 0.66 1.38 2.99 � � � �Aetideus armata � � � � 9 0.45 1.97 7.75 � � � �Aetideopsis sp. 1 0.00 0.00 0.02 � � � � � � � �Chiridiella sp. � � � � 1 0.29 0.43 1.71 � � � �Euchirella sp. 1 0.00 0.00 0.02 � � � � � � � �Gaetanus sp. 1 0.01 0.01 0.34 2 1.33 0.61 2.51 � � � �Pseudochirella sp. 1 0.00 0.01 0.34 � � � � � � � �Other Aetideidae 71 1.28 2.84 24.2 22 3.13 4.84 16.5 6 0.26 1.80 18.6Calanus sp. 164 9.00 16.3 44.4 47 5.88 7.81 22.6 � � � �Calanus finmarchicus 388 27.9 51.4 71.7 94 8.14 12.2 14.8 � � � �Other Calanidae 116 2.88 4.56 5.80 11 1.18 1.87 7.68 46 1.33 7.16 54.8Candacia sp. � � � � 39 1.13 6.99 65.4Candacia armata 1 0.00 0.00 0.02 � � � � � � � �Other Candaciidae 5 0.04 0.06 0.07 � � � � � � � �Euchaeta sp. 1 0.00 0.00 0.02 � � � � � � � �Paraeuchaeta sp. 1 0.01 0.00 0.01 � � � � 1 0.09 0.12 2.06Paraeuchaeta norvegica 37 5.99 1.87 20.6 17 14.7 3.88 17.7 6 0.87 0.70 8.22Paraeuchaeta tonsa 1 0.00 0.00 0.02 � � � � 1 0.09 0.12 2.06Other Euchaetidae 22 0.37 0.87 11.6 12 3.20 3.30 6.84 � � � �Heterorhabdus sp. 10 0.04 0.13 0.67 3 0.24 0.53 1.62 � � � �Heterorhabdus compactus 1 0.00 0.00 0.02 � � � � � � � �Heterostylites longicornis 1 0.00 0.00 0.02 � � � � � � � �Heterostylites sp. 12 0.00 0.03 0.20 1 0.26 0.43 1.50 � � � �Other Heterorhabdidae � � � � 1 0.01 0.15 1.54 � � � �Metridia sp. 87 0.21 1.25 4.21 71 6.27 12.2 22.5 � � � �Metridia curticauda 1 0.00 0.01 0.13 � � � � � � � �Metridia lucens 1 0.00 0.00 0.03 46 4.79 7.84 6.45 � � � �Pleuromamma sp. 218 1.42 4.18 39.4 37 4.67 8.45 27.2 82 2.17 17.2 80.2Pleuromamma abdominalis 5 0.01 0.02 0.15 1 0.11 0.19 1.02 11 0.19 1.28 8.22Pleuromamma borealis 5 0.01 0.02 0.08 � � � � � � � �Pleuromamma gracilis 2 0.00 0.00 0.04 � � � � � � � �Pleuromamma robusta 1 0.00 0.00 0.02 � � � � � � � �Pleuromamma xiphias 1 0.00 0.00 0.02 � � � � � � � �Other Metridinidae 48 0.19 1.03 3.87 20 3.06 4.54 17.4 � � � �Paracalanus sp. 1 0.00 0.00 0.02 � � � � � � � �Other Spinocalanidae 1 0.00 0.00 0.02 � � � � � � � �Other Calanoida 129 1.26 3.04 8.86 50 7.95 9.65 38.2 39 1.55 7.53 56.4CyclopoidOncaea sp. 21 0.02 0.77 9.84 2 0.02 0.29 2.62 27 0.06 5.36 55.2Poecilostomatoida 1 0.00 0.00 0.02 � � � � � � � �Sapphirina sp. 1 0.00 0.01 0.06 � � � � � � � �Other Copepoda 20 0.52 0.98 12.4 10 1.39 2.11 10.4 4 0.15 1.02 14.8

Amphipoda 19 0.34 0.12 2.21 � � � � 17 4.92 5.12 51.6Themisto sp. 10 0.09 0.06 0.40 � � � � � � � �Themisto compressa 2 0.10 0.07 1.64 � � � � � � � �Phronima sp. 1 0.45 0.11 0.30 � � � � � � � �Other Hyperiidae 14 0.21 0.28 1.37 � � � � 1 0.25 0.27 1.83

Euphausiacea 34 28.7 1.82 17.3 14 24.9 2.61 13.4 34 68.8 7.49 56.6Euphausiidae 25 8.35 0.51 4.08 � � � � � � � �

Myodocopoda 247 3.11 3.72 19.2 55 4.87 9.70 35.2 162 14.4 37.1 80.4Conchoecia sp. 2 0.01 0.01 0.04 � � � � � � � �Conchoecia magna 2 0.01 0.01 0.04 � � � � � � � �Conchoecetta acuminate 1 0.00 0.00 0.02 � � � � � � � �Conchoecilla daphnoides 1 0.00 0.00 0.02 � � � � � � � �Other Conchoecinae 6 0.01 0.01 0.10 13 1.52 2.30 4.26 � � � �

Pteropoda 1 0.00 0.01 0.02 � � � � � � � �Limacina sp. 1 0.00 0.01 0.02 � � � � � � � �Cavoliniidae � � � � � � � � 2 0.00 0.23 2.06

Gelata 6 0.10 0.37 1.02 � � � � � � � �Thaliacea 1 0.01 0.11 0.30 � � � � � � � �

Chaetognatha 13 6.08 1.05 5.48 � � � � � � � �Polychaeta 1 0.01 0.01 0.05 � � � � � � � �Osteichthyes 2 0.08 0.04 0.00 � � � � 1 3.49 0.20 5.40Crustacea 8 0.07 0.05 0.18 2 0.51 0.55 2.14 � � � �Unidentified prey 23 0.79 1.56 11.8 1 0.40 0.17 2.05 2 0.14 0.31 7.46

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116 107

between night and day integrated myctophid biomass in the0–200 m depth interval.

A sensitivity analysis was used to estimate CO2, DOC, and POCflux using a range of values where available (Table 3). Respiratoryflux for all myctophid species at ridge section r was calculatedusing the following equation (Dam et al., 1995):

Fr ¼ BrRr12 ð5Þwhere Fr is the CO2 flux (mg C m�2 d�1), Br is the migratorbiomass integrated to 200 m (mg DWm�2), Rr is the weight-specific migrator respiration rate (mg C mg DW�1 h�1) at tem-peratures experienced during day time at depths of 200–750 m,and 12 is the assumed number of hours spent at depth over a24-h day.

The term R was calculated using the myctophid oxygen con-sumption vs. temperature (1C) regression reported in Donnelly andTorres (1988): y¼(0.016 n temperature)�0.07, where y is oxygenconsumption in units of ml O2 mg WW�1 h�1 converted to CO2

respiration in units of mg C mg DW�1 h�1 using carbon andoxygen atomic ratios. A respiratory quotient (RQ; the ratio ofoxygen consumed to carbon dioxide released) was used in thecalculation of R. A common RQ value for zooplanktivorous fishes is0.8 (Brett and Groves, 1979); however, a range of 0.7–1 was useddue to the lack of myctophid-specific data. DOC excretion data for

fishes are lacking, so the relationship of CO2 respiration to DOCexcretion in zooplankton (DOC excretion¼31% of CO2 respiration)reported by Steinberg et al. (2000) was used to estimate DOCexcretion in myctophids, with a range of 20–40% used in thesensitivity analysis. POC egestion at depth was calculated for B.glaciale and P. arcticum using the carbon conversions discussedabove. We assumed that 100% of stomach and intestinal contentsof fish caught at the surface would be released below 200 m basedon myctophid gut clearance times ranging from 4 to 40 h(Pakhomov et al., 1996, Pepin, 2013). Similar to Eq. (5) above,POC egestion at depth (mg C m�2 d�1) was calculated by multi-plying prey carbon per mg fish DW by the integrated fish biomassat the RR or AZ and by 12 h. Myctophid dry weight was deter-mined using a wet weight-standard length regression for eachspecies (Fock and Ehrich, 2010) and a wet weight–dry weight ratio(DW/WW¼22.64720%) based on an average of compiled wetweight–dry weight ratios for many individual myctophid species(Carmo pers. comm.).

3. Results

3.1. General diet description

Fifty-nine different prey types were identified in 201 nonemptyB. glaciale stomachs to an array of taxonomic levels depending onthe extent of digestion. Copepods constituted the bulk of the dietby dry weight (52%), were the most frequently occurring preycategory (93%), and were the most abundant prey by number(90%). The copepod Calanus finmarchicus was the predominantorganism in the diet of B. glaciale and made up over one quarter ofthe diet by dry weight alone. Euphausiids were another majorcomponent of the diet, constituting 37% of the diet by dry weight.The remaining prey categories constituted 6% or less of the dietby dry weight, and included chaetognaths, ostracods, amphipods,gelatinous zooplankton, fishes, polychaetes, pteropods, anddigested crustaceans.

The diet of P. arcticum comprised 26 different prey types from74 nonempty stomachs and contained primarily copepods andeuphausiids by dry weight (68% and 25%, respectively). Nearly allP. arcticum stomachs contained copepods (93%) with the largecopepod Paraeuchaeta norvegica constituting the highest propor-tion of copepod dry weight (15%). Ostracods, digested crustaceans,and unidentified prey were the only other prey found in the diet ofP. arcticum.

Eighteen different prey types from 28 nonempty stomachswere identified in the diet of H. hygomii. Euphausiids constitutedthe highest proportion of the diet by dry weight (53%) with a mid-level frequency of occurrence (57%) and a relatively low percent bynumber (7%). Ostracods were consumed frequently (84%) and inhigh numbers (49%), while copepods, mainly Pleuromamma spp.,Candacia spp., and euchaetid species, were the most frequentlyconsumed prey category (84%) and made up half of the diet bynumber. Fishes, amphipods, pteropods, and unidentified prey eachmade up 5% or less by dry weight, although amphipods werefound in over half of stomachs.

3.2. Ontogenetic and spatial changes in diet

The sizes of B. glaciale included in this study ranged from 11 to67 mm standard length (Fig. 2). Aside from a lack of euphausiidsin the diets of myctophids o20 mm (cluster A), there were nofurther detectable ontogenetic changes in prey type consumedover the size classes examined as indicated by cluster analysis(Fig. 3). The diets of B. glaciale in cluster B contained the highestproportion of euphausiid weight, while those in cluster C

Table 2Evacuation rates at minimum, average, and maximum water temperatures (200–750 m) and daily consumption at each ridge section (RS) (RR, Reykjanes Ridge;CGFZ, Charlie–Gibbs Fracture Zone; FSZ, Faraday Seamount Zone; and AZ, AzoreanZone) by individual myctophids (μg DW d�1) and by the uncorrected and correctedbiomass (corrected biomass adjusted for 14% gear efficiency) of all myctophidspecies (μg DW m�2 d�1) at each ridge section integrated 0–2300 m using theaverage consumption per unit fish biomass based on Benthosema glaciale stomachcontent weights. Minimum individual consumption was always less than1 μg DW d�1.

RS T 1C Evac rate(h�1)

Individual Total uncorrectedbiomass

Total correctedbiomass

Avg Max Min Avg Max Min Avg Max

RR 4.2 0.13 11 119 6 32 162 41 231 11556.6 0.15 13 141 7 42 194 49 300 13869.6 0.19 16 174 8 323 2264 60 2310 16,173

CGFZ 3.8 0.12 7 21 6 26 52 44 188 3694.9 0.13 7 22 7 28 103 48 203 7378.5 0.17 9 29 9 37 103 62 264 737

FSZ 4.5 0.13 1 4 2 5 51 11 39 3637.6 0.16 2 5 2 7 63 14 49 45111.7 0.22 2 7 3 9 75 18 64 536

AZ 7.1 0.16 0 0 0 0 5 0 4 3311.8 0.22 0 0 0 1 7 0 5 4715.6 0.29 0 1 0 1 9 0 7 66

Table 3Minimum and maximum values of parameters used in active carbon transportanalysis (RR, Reykjanes Ridge; AZ, Azorean Zone; WW, wet weight; and DW, dryweight).

Parameter Minimum Maximum

Temperature (1C) RR 200–750 m 5 10Temperature (1C) AZ 200–750 m 7 16Respiratory quotient 0.7 1O2 consumption slope 0.012 0.02O2 consumption intercept �0.0875 �0.0175CO2:DOC ratio 0.2 0.4Myctophid DW:WW (%) 18.1 27.2

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116108

contained a smaller proportion. The size distribution of P. arcticumwas 18–45 mm standard length (Fig. 2). The cluster analysis andscree plot indicated there was no ontogenetic change in the diet

(data not shown). Due to the lack of evidence of ontogenetic shiftin the diet of B. glaciale and P. arcticum, fish size was not includedas an explanatory variable in subsequent analyses. The sizedistribution of H. hygomii was 28–56 mm standard length (Fig. 2)but the small sample size of H. hygomii did not allow for clusteranalysis.

Canonical correspondence analysis (CCA) indicated significantB. glaciale dietary changes in relation to ridge section (p¼0.005)and time of day (p¼0.025), but nonsignificant changes in relationto depth zone (Fig. 4). The three explanatory variables included inthe CCA, depth, ridge section, and time of day, accounted for 30%of the variability in the diet, collectively. The first and secondcanonical axes accounted for 34% and 29% of the explainablevariation, respectively. Ridge section corresponded more closelywith the first canonical axis than the second and accounted for a

Num

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45−49

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60−64

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.9

Standard Length (mm)

n = 265

Benthosema glacialeN

umbe

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peci

men

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.9

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.9

Standard Length (mm)

n = 76

Protomyctophum arcticum

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.9

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Standard Length (mm)

n = 39

Hygophum hygomii

Fig. 2. Standard length (mm) frequency histograms for myctophids included in thisstudy. n is the number of each species dissected.

10−1

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rage

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Size Class (mm)

A B C

2 4 6 8 10

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Number of Clusters

Ave

rage

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tanc

e B

etw

een

Clu

ster

s

Fig. 3. Cluster diagram (A) and scree plot (B) for Benthosema glaciale. The clusterdiagram represents the relationships among the diet compositions of 5 mm sizeclasses of B. glaciale. The scree plot was used to determine the number of clustersinto which the size classes of B. glaciale should be grouped.

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116 109

greater proportion of the explainable variation associated withthat axis.

The diet of B. glaciale differed among ridge sections in that preytypes constituting the bulk of the diet from the three northernridge sections were similar to each other, but different from preytypes from the southern AZ (Fig. 5A). The diets of B. glaciale fromthe RR, CGFZ, and FSZ comprised mainly euphausiids – 35%, 44%,and 65% by dry weight, respectively. The copepod C. finmarchicusranked second in the RR and CGFZ, constituting 31% and 25% of thediet by weight, respectively. The abundance of C. finmarchicus, thenumerically dominant calanoid copepod north of the SPF and inthe diet of B. glaciale, declined by two orders of magnitude to thesouth of the front and was not identified in the diets from the AZ.The diets of B. glaciale from the AZ differed in that ostracods madeup 59% of the diet by dry weight. Pleuromamma copepods (7%)were the only other prey to make up greater than 5% of the diet bydry weight in B. glaciale from the AZ.

The diet of B. glaciale summarized by dry weight differed withtime of day. Stomach contents of fish collected during the daywere comprised mainly of C. finmarchicus (31%) and euphausiids(29%), whereas at night copepods of the family Calanidae were theprimary prey (42%), and at dawn chaetognaths (67%) were thepredominant prey (Fig. 5B). Calanus finmarchicus, pteropods, andfish prey were only identified in specimens collected during theday and polychaetes were only found in dawn samples.

CCA of P. arcticum diet indicated depth zone (p¼0.03) was theonly significant factor; ridge section (p¼0.46) and time of day(p¼0.23) were not significant. The three explanatory variablesincluded in the CCA accounted for 38% of the variability in the diet,collectively (Fig. 6) and the first and second canonical axesaccounted for 38% and 32% of the explainable variation, respec-tively. Depth zone corresponded more closely with the secondcanonical axis. The main difference in P. arcticum diet by dryweight in relation to depth zone was the high proportion ofeuphausiids (31%) in fish collected from depth zone 2 (200–750 m) and the absence of euphausiids in fish from depth zone1 (0–200 m; Fig. 7). The main components in the diets by dry

weight of fish from depth zone 1 were the copepod Metridia sp.(17%), ostracods (16%), C. finmarchicus (13%), and copepods of thefamily Aetideidae (12%).

−2.0 −1.5 −1.0 −0.5 0.0 0.5 1.0

−1.5

−1.0

−0.5

0.0

0.5

1.0

Aetideidae

Amphipoda

Calanidae

Other Calanoida

Calanus finmarchicus

Calanus sp.

Candaciidae

Chaetognatha

CopepodaCrustacea

Euchaetidae

Euphausiacea

Euphausiidae

GelataHeterorhabdus sp.

Heterostylites sp.

Hyperiidae

Metridia sp.

Metridinidae

Myodocopoda

Oncaea sp.

Paraeuchaeta norvegica

Pleuromamma sp.

Polychaeta

PteropodaOsteichthyes

Unidentified prey

DZ 1

DZ 2

DZ 3

AZ

CGFZ

FSZ

RR

Day

NightDawn

Canonical Axis 1

Can

onic

al A

xis 2

Fig. 4. Canonical correspondence analysis biplot for Benthosema glaciale. Boldedlabels represent the centroids for each level of the ridge section (Reykjanes Ridge,RR; Charlie–Gibbs Fracture Zone, CGFZ; Faraday Seamount Zone, FSZ; AzoreanZone, AZ) time of day, and depth zone (0–200 m, DZ 1; 200–750 m, DZ 2; 750–1500 m, DZ 3) explanatory variables. Points represent prey types in the diet. Thecanonical axes represent linear combinations of the explanatory variables. Ridgesection and time of day were significant at α¼0.05.

010203040506070

Reykjanes Ridgen=84

010203040506070

Perc

ent W

eigh

t

Charlie Gibbs Fracture Zonen=40

010203040506070

Faraday Seamount Zonen=66

Aet

idei

dae

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anid

aeC

alan

us sp

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. fin

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chic

usEu

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idae

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eriid

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Gel

ata

Cha

etog

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lych

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eich

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rey

010203040506070

Azorean Zonen=64

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20

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80 Dayn=151

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ent W

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Nightn=68

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idei

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. fin

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lych

aeta

Ost

eich

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ntifi

ed P

rey

020406080 Dawn

n=12

Fig. 5. Diet composition (percent weight) of Benthosema glaciale presented by(A) ridge section and (B) time of day. Error bars represent standard error of thepercent weight values of each prey type in the diet of B. glaciale calculated fromvariance estimates (Eq. 3). n is the number of stomachs dissected from each ridgesection or time of day.

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116110

3.3. Gastric evacuation and daily consumption

A range of gastric evacuation rates was calculated for eachmyctophid species using minimum, average, and maximum watertemperatures experienced in the 200–750 m depth zone in eachridge section. From the northernmost ridge section to the south-ernmost, average water temperatures (1C) were 6.6 (RR), 4.9(CGFZ), 7.6 (FSZ), and 11.8 (AZ) (Table 3), with the decline intemperature at the CGFZ due to the unique physical characteristicsof the Subpolar Front present in this area (Søiland et al., 2008).Myctophid evacuation rates ranged from 0.13 to 0.29 h�1 (Table 2).The average total dry weight of prey in the stomachs of B. glaciale(μg DW prey fish�1) was highest at the RR (3.6, range 0–39) and

for P. arcticum at the CGFZ (0.09, range 0.003–0.37). H. hygomii wasonly caught at the AZ and the average total weight of prey in thestomachs was 0.92 μg DW prey fish�1 (range 0.24–1.97).

Estimated daily consumption of prey (μg DWm�2 d�1)inferred for all MAR myctophid species at average water tempera-tures based on B. glaciale consumption rates was 42.0 at the RR,28.4 at the CGFZ, 6.83 at the FSZ, and 0.72 at the AZ. Dailyconsumption in proportion to myctophid body weight was alwaysless than 1% for each species regardless of ridge section, with B.glaciale from the RR from 200 to 750 m having the highestconsumption of 0.7% of body weight per day at maximum watertemperatures. The daily consumption (μg DWm�2 d�1) usingsampling efficiency corrected myctophid biomass values averaged300 at the RR, 203 at the CGFZ, 48.8 at the FSZ, and 5.12 at the AZ.Using integrated zooplankton biomass values from Gallienne et al.(2001) for RR estimates and Steinberg et al. (2012; http://bats.bios.edu/) for AZ estimates and average myctophid consumption rates,results in an estimated removal of o1% of zooplankton biomass ateach ridge section every night.

3.4. Active carbon export by diel vertical migration

Myctophid biomass in the surface 200 m increased at night by3.1-fold at the RR and 3.8-fold at the AZ, indicating diel verticalmigration (Fig. 8). This resulted in a migrant myctophid biomass(uncorrected for gear sampling efficiency) of 5.2 and 40 mg C m�2

in the RR and AZ, respectively. Respiration of CO2 at depth by themigrant myctophid biomass at the RR ranged from 0.01 to 0.03(average 0.01) mg C m�2 d�1 (minimum water temperature from200 to 750 m in the RR was lower than the minimum tempera-tures used to generate the oxygen consumption regression inDonnelly and Torres (1988) and thus the minimum estimate abovemay be unreliable) while respiration at the AZ ranged from 0.05 to0.27 (average 0.13) mg C m�2 d�1 (Table 4). Myctophid excretionranged from o0.01 to 0.01 mg C m�2 d�1 at the RR and from 0.01to 0.11 mg C m�2 d�1 at the AZ. Export of POC by myctophidegestion at depth was low, o0.01 mg C m�2 d�1, regardless ofridge section or myctophid species used to estimate weight-specific egestion rate, and considering the range of values deter-mined in the sensitivity analysis. Estimated total carbon transportby the migrant myctophid biomass in the RR ranged from 0.01 to0.04 (average 0.02) mg C m�2 d�1 and in the AZ ranged from 0.06to 0.38 (average 0.17) mg C m�2 d�1. Using sampling efficiency-corrected migrant myctophid biomass (38 and 285 mg C m�2 inthe RR and AZ, respectively), active transport ranged from 0.04 to0.26 mg C m�2 d�1 in the RR and from 0.40 to 2.78 mg C m�2 d�1

in the AZ, equivalent to 0.01–3.2% of sinking POC at 150 m and0.05–7.5% at 300 m (based on POC flux values from studies in theNorth Atlantic during April and May, Table 4).

4. Discussion

4.1. General diet description

Of the three myctophid species included in this study, more isknown about the feeding ecology of B. glaciale than P. arcticum orH. hygomii. The diet of B. glaciale from the MAR observed in thisstudy consisted predominantly of copepods by dry weight, fre-quency of occurrence, and abundance. Calanus finmarchicus andeuphausiids made up the bulk of the diet by dry weight, withmany other copepod taxa, amphipods, ostracods, chaetognaths,pteropods, polychaetes, fishes, and unidentified gelatinous zoo-plankton consumed as well. Myctophids consume gelatinous prey,although how commonly they do so remains unclear. Severalstudies from the Gulf of Mexico reported some larval and adult

Fig. 6. Canonical correspondence analysis biplot for Protomyctophum arcticum.Explanatory variables include ridge section, time of day, and depth zone. Depthzone was significant at α¼0.05. For description of explanatory variables see Fig. 4.

0

20

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Aet

idei

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Euph

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rust

acea

Uni

dent

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Pre

y

Depth zone 1, n = 15Depth zone 2, n = 54

40

20

0

Perc

ent W

eigh

t

Fig. 7. Diet composition (percent weight) of Protomyctophum arcticum, presentedby depth zone (depth zone 1, 0–200 m; depth zone 2, 200–750 m). Error barsrepresent standard error of the percent weight values of each prey type in the dietof P. arcticum calculated from variance estimates (Eq. 3). n is the number ofstomachs dissected from each depth zone.

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116 111

myctophid species fed on gelatinous prey, with some larvaefeeding almost exclusively on gelatinous zooplankton (Hopkinsand Gartner, 1992, Conley and Hopkins, 2004). Hopkins andGartner (1992) reported gelatinous prey in the diet of Benthosemasuborbitale; however, to our knowledge, gelatinous prey has notpreviously been reported in the diet of B. glaciale. Gelatinous preywas identified in the stomachs of seven B. glaciale 440 mm fromthe MAR, equating to less than 1% of the numerical abundance ofprey in the diet. Due to the rapid digestion of gelatinous material,this represents an underestimate of gelatinous zooplankton in thediet of this species (Arai et al., 2003). The diet of B. glaciale fromthe MAR was similar to the results of other studies in thatcopepods (predominantly C. finmarchicus, Pleuromamma spp.Metridia spp., and Paraeuchaeta norvegica) comprised the bulk ofthe diet, with euphausiids, ostracods, amphipods, pteropods,chaetognaths, and fish also consumed (Gjøsæter, 1973; Kinzer,1977; Kawaguchi and Mauchline, 1982; Roe and Badcock, 1984;Petursdottir et al., 2008; Pepin, 2013).

The diet of P. arcticum from the MAR was also comprisedmainly of copepods, with P. norvegica constituting the bulk of thecopepod component. Euphausiids and ostracods were the onlyother identifiable prey in the diet. In a study from the RockallTrough in the North Atlantic, the diet of P. arcticum was alsocomprised mainly of copepods, specifically Pleuromamma spp.,(Kawaguchi and Mauchline, 1982). In the Davis Strait west ofGreenland, C. finmarchicus was the only identifiable prey(Sameoto, 1989). H. hygomii fed mainly on euphausiids andcopepods; however, fish prey were also abundant, constituting5% numerically. In previous studies at Great Meteor Seamount andin the Gulf of Mexico, H. hygomii fed on a wide variety of preyincluding copepods, euphausiids, and gelatinous prey (Hopkinsand Gartner, 1992; Pusch et al., 2004).

4.2. Ontogenetic and spatial changes in diet

Ontogenetic changes in the diet of P. arcticum were notidentified by cluster analysis, although there was a slight tendencyfor larger P. arcticum to consume larger prey such as euphausiidsand the copepod P. norvegica, while smaller P. arcticum consumedprimarily small copepods. The grouping of B. glaciale size classesin the cluster analysis was driven primarily by the weight ofeuphausiids in the diet and did not indicate ontogenetic changes,although the smallest size classes did group together based on alack of euphausiid consumption and all size classes above 20 mmdid consume euphausiids (Fig. 3). The presence of euphausiids inthe diets of smaller B. glaciale from the MAR, which has not beenpreviously reported in other regions (Kinzer, 1977; Kawaguchi andMauchline, 1982), in addition to the presence of gelatinouszooplankton, suggests the diet of MAR myctophids may be distinctcompared to those in off ridge waters.

The diets of B. glaciale, P. arcticum, and H. hygomii are influ-enced by the prey fields which are markedly different to the northand south of the Sub-Polar Front (SPF). Gaard et al. (2008) foundthat the SPF appeared to act as a boundary to the horizontaldistribution of several copepod genera, with the northward dis-tribution of southern copepod genera restricted more so than thereverse. CCA revealed the diet of B. glaciale to be influencedprimarily by ridge section, which serves as a proxy for latitude,rather than by depth or time of day. This suggests that hydro-graphic features, such as the Sub-Polar Front and physical proper-ties of water masses, may play a greater role in myctophid dietthan the MAR itself, if explanatory variables in the diet ofB. glaciale are applicable to other myctophid species. This may betrue more so for mesopelagic myctophids than bathypelagic fishesbecause the MAR in the study area resides primarily below1000 m, deeper than the range of most vertical migrators.

Aside from ridge section, patterns in the diet with respect totime of day were also present; although, such patterns weredriven primarily by a few prey species and were not observedfor the diet as a whole. The absence of C. finmarchicus from nightand dawn samples, while constituting a third of the diet by weightduring the day, contributed to the significant differences inB. glaciale diet with respect to time of day. The absence ofC. finmarchicus from the diet at night and dawn could be due tomismatch in vertical distribution of predator and prey, althoughGaard et al. (2008) reported C. finmarchicus was present from0–2500 m at the MAR during the same sampling period. Alter-natively, the absence of C. finmarchicus could be an artifact of poortaxonomic resolution in prey identification, as copepods of thefamily Calanidae made up 42% of night diets by weight. Althoughchaetognaths made up a greater proportion of the diet by weightof B. glaciale during dawn (67%) than other times of day (4% or lessin day and night samples), this trend is driven by two particularly

0 50 100 150

NightDayRR Biomass (mg C m−2)

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1500

2300

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th (m

)

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150 100 50 0

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200

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1500

2300

Dep

th (m

)

Fig. 8. Vertical distribution of all myctophid species (uncorrected for gear effi-ciency) during day and night from (A) the Reykjanes Ridge (RR) and (B) the AzoreanZone (AZ). Error bars represent standard error.

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116112

large chaetognaths found in fish stomachs at dawn and may not beindicative of diel diet changes.

Depth was the only significant explanatory variable in the dietof P. arcticum as indicated by CCA; although, P. arcticum was onlycollected from r750 m and, as in the case of B. glaciale, dietarypatterns may not be directly attributable to the MAR itself. Themain difference in P. arcticum diet between depth zones 1 and2 was the presence of euphausiids only in stomachs collectedduring the day in the deeper depth zone 2, possibly due toeuphausiid diel vertical migration. However, abundances ofeuphausiids were much higher in depth zone 2 than in depthzone 1 during both day and night (MAR-ECO unpublished data).Alternatively, fish size may be the underlying factor dictatingeuphausiid consumption at depth. Larger predators are capableof consuming larger prey, and larger fish of a species are com-monly found deeper than smaller individuals (Collins et al., 2008;Sweetman et al., 2013). However, there was only a 4 mm increasein average P. arcticum size from depth zone 1 (28.4 mm SL) todepth zone 2 (32.1 mm SL) and the size range of P. arcticum thatconsumed euphausiids encompassed the average length of fishesin each depth zone (28–44.5 mm SL). Protomyctophum arcticumdiet characteristics with respect to depth included aetideidcopepods, C. finmarchicus, Metridia sp., and ostracods, all of whichare known vertical migrators (Al-Mutairi and Landry, 2001;Irigoien et al., 2004), and which constituted a considerably greaterproportion of the diet by weight in depth zone 1, while P. norvegicamade up a greater proportion in depth zone 2. Other prey weregenerally consumed in similar proportions at both depths.

An alternative to significant diet differences being due to thevertical distribution of prey is differences in the vertical dis-tribution of P. arcticum. Results from Nafpaktitis et al. (1977) andHulley (1984) suggested P. arcticum in the North Atlantic mayexhibit a weak diel vertical migration, with depths of P. arcticummaximum abundance during the day vs. night of 350 m vs.250 m, respectively, and depth ranges of occurrence of 250–850 m vs. 90–325 m, respectively. During the day, P. arcticumfrom the MAR exhibited typical patterns of abundance corre-sponding to diel vertical migration, with abundance in depthzone 2 more than three times that in depth zone 1. However,night time abundance was nearly equal in depth zones 1 and 2,suggesting a sizeable proportion of the P. arcticum populationremains at depth and does not migrate (Watanabe et al., 1999,Kaartvedt et al., 2009, Dypvik et al., 2012). This is supported byCook et al. (2013) who report approximately two-thirds of the

P. arcticum population remained at depth at night based onsamples collected from a subsequent MAR-ECO expedition tothe CGFZ in 2009.

4.3. Daily consumption

The maximum daily consumption as a percentage of dry bodyweight for myctophids in this study was 0.7%, which agrees wellwith the estimates of Pepin (2013) who found average rations of B.glaciale to be less than 1% of body weight per day and hypothe-sized that this species does not feed daily, but once every twodays. Although a variety of methods has been used and directcomparisons are not possible, the consensus is that myctophidsgenerally consume o1–6% of dry body weight per day, with mostestimates closer to 1% (see Table 6.2 in Brodeur and Yamamura,2005, and references therein). The similarity of these results to offridge estimates indicate that the MAR may not significantlyinfluence the daily consumption of myctophids, although dailyconsumption estimates for MAR myctophids presented here arelikely to be underestimated as a result of the sampling designemployed on the G.O. Sars cruise. Shallow depths were sampledfirst and, thus, myctophids collected in depth zones 1 and 2 wouldcontinue digesting for many hours after capture while the deeperdepths were sampled. This prolonged digestion would result in anunderestimation of prey abundance in stomachs and, conse-quently, underestimation of prey weight as a percentage of fishbody weight.

Estimated removal rates at the MAR were comparable withestimates by Pepin (2013) who reported B. glaciale fed primarily oncopepods and consumed 0.002–1.8% (midpoint 0.15%) of copepodsin the Labrador Sea per day. Consumption rates reported by Pepin(2013) and in the current study are similar to or lower than dailyzooplankton removal rates by myctophids reported in previousstudies: 1–4% of zooplankton standing stock in the upper 150 m inthe western North Pacific (Watanabe et al., 2002), 2% in the upper200 m in the Gulf of Mexico (Hopkins and Gartner 1992), and5–20% in the upper 300 m in the Southern Ocean (Pakhomov et al.,1999). Minimal feeding impact of myctophids on zooplanktonobserved in our study could be a result of the time of yearsampling occurred, which likely coincided with maximum zoo-plankton abundance following the spring bloom. The impact ofmyctophid predation at the MAR has the potential to be greater inother seasons when zooplankton abundance is lower.

Table 4Active transport of carbon (mg C m�2 d�1) by diel migrating myctophids from the Reykjanes Ridge (RR) and Azorean Zone (AZ). Integrated (0–200 m) migrant myctophidbiomass (mg C m�2), uncorrected and corrected for 14% gear efficiency, was 5.2 and 38 in the RR and 40 and 285 in the AZ, respectively. Active transport calculated usingboth uncorrected and corrected myctophid biomass is presented. Active transport of CO2 and dissolved organic carbon (DOC) is for the 0–200 m integrated biomass of allmyctophid species combined. Active transport of particulate organic carbon (POC) is the average carbon content of prey from night time 0–200 m Benthosema glaciale dietsmultiplied by the 0–200 m integrated biomass of all myctophid species combined. Minimum, average, and maximum values were obtained from a sensitivity analysis ofcarbon transport parameters. Total myctophid carbon export across 200 m using the corrected myctophid biomass is compared to average POC flux in the North AtlanticOcean from different locations and depths n during spring (April and May), i.e., (active transport/sediment trap POC flux)�100%; % POC.

Ridge Section Uncorrected biomass Corrected biomass

CO2 DOC POC Total CO2 DOC POC Total % POC

RRAverage 0.013 0.004 o0.001 0.017 0.090 0.028 o0.001 0.118 0.04–0.3Min 0.005 0.001 o0.001 0.006 0.030 0.006 o0.001 0.036 0.01–0.1Max 0.027 0.010 o0.001 0.037 0.190 0.073 o0.001 0.263 0.1–0.7

AZAverage 0.129 0.040 o0.001 0.169 0.920 0.290 o0.001 1.210 0.5–3.3Min 0.046 0.009 o0.001 0.055 0.330 0.070 o0.001 0.400 0.2–1.2Max 0.271 0.110 o0.001 0.381 1.940 0.840 o0.001 2.780 1.1–7.5

nPOC flux ranged from 86 to 259 mg C m�2 d�1 at 150 m and from 37 to 72 mg C m�2 d�1 at 300 m (Bender et al., 1992, Buesseler et al., 1992, Ducklow et al., 1993, Harrisonet al., 1993, Martin et al., 1993). Sampling during the G.O. Sars cruise was performed during a post-bloom period and during which passive POC flux could be lower thanduring the spring bloom.

J.M. Hudson et al. / Deep-Sea Research I 93 (2014) 104–116 113

4.4. Active carbon transport by myctophid diel vertical migration

We compare our estimates of myctophid active carbon trans-port to passive POC flux measured by sediment traps, and tozooplankton active transport, to explore their relative importanceas components of the biological pump (Steinberg et al., 2000;Hidaka et al., 2001). Diel vertically migrating zooplankton con-tribute to the vertical export of carbon from the euphotic zonethrough mortality, respiration, excretion, and egestion at depthduring the day of food consumed in surface waters at night(Longhurst et al., 1990; Dam et al., 1995; Zhang and Dam 1997;Steinberg et al., 2000, 2008; Al-Mutairi and Landry 2001;Schnetzer and Steinberg 2002; Kobari et al., 2008). This ‘activetransport’ could be an important source of carbon for non-migrating mesopelagic zooplankton, and for mesopelagic bacteria,which are ultimately reliant on surface-derived production(Steinberg et al., 2008). Diel vertically migrating fishes may alsocontribute to active transport of carbon, and as myctophids are themost abundant vertically migrating mesopelagic fishes at the MARand many other regions, it is important to consider their role inthe biological pump. Indeed, acoustic estimates of mesopelagicfish biomass by Irigoien et al. (2014), although not ground-truthedby net sampling, are an order of magnitude higher than reportedin the classic study of Gjøsaeter and Kawaguchi (1980) whichwould significantly increase contributions by vertically migratingfishes to carbon flux.

Integrated (0–200 m) migrant myctophid biomass (mg C m�2),uncorrected and corrected for sampling efficiency, was 5.2 and 38in the RR and 40 and 285 in the AZ, comparable with total fishbiomass estimates in the North Atlantic by Angel and Pugh (2000)of up to ca. 40 mg C m�2 in the top 200 m. Active transport of CO2,DOC, and POC during summer by the corrected MAR myctophidbiomass was as much as 3.2% of passively sinking POC in the NorthAtlantic at 150 m and 7.5% at 300 m. Although not quantified inour study, mortality of diel migrating myctophids at depth wouldfurther increase export, with previous such estimates for fishesranging from o0.1 to 20.3 mg C m�2 d�1 (Williams and Koslow,1997; Angel and Pugh, 2000; Davison et al., 2013). Another studyinvestigating carbon export by myctophids in the western equa-torial North Pacific reports myctophid biomass (uncorrectedfor sampling efficiency) of 249–462 mg C m�2 (0–160 m) andactive transport through respiration and egestion of 1.2–2.2 mg C m�2 d�1, equivalent to 2.0–3.7% of passively sinkingPOC (Hidaka et al., 2001, stations 15 and 16). Hidaka et al.,(2001) adopted the 0.14 sampling efficiency estimated by Koslowet al. (1997), which significantly increased their myctophid bio-mass estimate (1778–3303 mg C m�2) and, subsequently, carbonexport (8.4–15.4 mg C m�2 d�1, 14.3–26.4% of sinking POC).Davison et al. (2013) estimated the average biomass of mesopela-gic fishes off the continental U.S. to be 24.7 g WW m�2 (correctedfor a sampling efficiency of 0.06) and mediates, on average, 15–17%of total carbon export. Approximately half of this export passesthrough vertically migrating fishes, over 90% of which are mycto-phids. The high myctophid biomass in both Pacific studies con-tributes to the considerably higher active carbon transportestimated there compared to the MAR. Myctophid active transportalong the MAR is also lower than the long-term (1994–2011)annual average zooplankton active transport in the subtropicalNorth Atlantic measured at the BATS station. There zooplanktontransported 4.1 mg C m�2 d�1 via respiration, excretion, and eges-tion at depth, which was on average 15% of sinking POC flux at150 m (Steinberg et al., 2012).

At deeper depths, active transport by myctophids becomesincreasingly important as myctophids, of which some species verti-cally migrate 1000 m or more (Fig. 8), have the potential to transporta greater proportion of sinking POC, due to the rapid decline of

sinking POC with increasing depth. As a rough comparison, Honjoand Manganini (1993) report passive POC flux at 1000 m in theNorth Atlantic during April of 4.1 mg Cm�2 d�1. Using corrected 0–200 m integrated MAR myctophid biomass, the myctophid carbonexport calculated in this study during summer would be equivalentto 1–73% of sinking POC at 1000 m. A few factors would decrease theamount of carbon transported to this depth, however. A smallerproportion of the migrating myctophid biomass resides at 1000 mduring the day, and greater migration distance means increased timefor digestion to occur resulting in a smaller proportion of POCactively exported out of the euphotic zone being released at1000 m (although active carbon transport is comprised predomi-nantly of respiration and excretion, with egestion of POC constitutinga small proportion). Nevertheless, the high proportion of carbonexported by myctophids in relation to POC flux at greater depthsreaffirms the potential importance of myctophids in the biologicalpump, and suggests that active transport by fishes should beconsidered in biogeochemical models.

5. Conclusions

The diet of the three species of myctophids from the MAR wasconsistent with previous investigations of these species in off-ridge areas of the North Atlantic Ocean. However, the mostabundant myctophid, B. glaciale, possessed unique dietary char-acteristics not observed in this species elsewhere, such as con-sumption of gelatinous prey, and of euphausiids and amphipodsearlier in the fish's life history (i.e., at smaller fish sizes), evidencethat the MAR may support a distinct food web structure. Samplingduring other times of the year is necessary to determine if the dietpatterns observed in this study during summer are characteristicof annual patterns at the MAR. Despite the temporal scale of thisstudy being limited to summer, our results will be useful forcomparison of MAR food web structure to that of continentalslope regions of the Atlantic. This study also provides the firstestimate of active carbon transport for Atlantic myctophids andfor a mid-ocean ridge. Carbon transport by myctophids at theMAR during summer was low compared to sinking POC flux inthe upper mesopelagic zone during the spring bloom at off ridgeareas, but may account for a greater proportion of exportedcarbon at lower mesopelagic and bathypelagic depths. Addi-tional spatial and temporal sampling and information on sam-pling efficiency of an array of trawl types are needed to developmore robust estimates of active carbon transport by myctophidsand other migrating fishes, resulting in a more comprehensiveview of the biological pump.

Acknowledgments

The authors acknowledge the crew of the R.V. G/O. Sars forexpert vessel operations during sample collection. Thanks are dueto I. Byrkjedal for shipping myctophid samples and to M. Vecchione,V. Carmo, and C. Sweetman for statistical and scientific guidance forthis research and manuscript. This research was funded by NSF,United States Ocean Sciences Division-Biological OceanographyProgram (Grant OCE 0623551 to T.T.S.) and by the VIMS Office ofAcademic Studies. This paper is Contribution no. 3388 of theVirginia Institute of Marine Science, College of William and Mary.

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