research article bounds on biomass estimates and energetic ...ctenophora were readily identi able in...

Research ArticleBounds on Biomass Estimates and Energetic Consequences ofCtenophora in the Northeast US Shelf Ecosystem

Michael D Ford1 and Jason S Link2

1 National Marine Fisheries Service 1315 East-West Highway Silver Spring MD 20910 USA2National Marine Fisheries Service 166 Water Street Woods Hole MA 02543 USA

Correspondence should be addressed to Michael D Ford michaelfordnoaagov

Received 19 July 2013 Revised 29 October 2013 Accepted 4 November 2013 Published 29 January 2014

Academic Editor Heinrich Huhnerfuss

Copyright copy 2014 M D Ford and J S Link This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Previous descriptions have noted that the stomach samples of spiny dogfish Squalus acanthias showed a major increase in theoverall occurrence and hence implied abundance of Ctenophora This apparent and persistent gelatinous zooplankton outbreakis increasingly more common in the worldrsquos oceans We briefly explore the energetic ramifications of ctenophores in the spinydogfish diet inferring that the presence of gelatinous zooplankton represents an ambient feeding strategy Relative to other preyctenophores are not a high energy density prey item However given varying assumptions of the amount of ctenophores consumedthey may be an important staple in the diet of spiny dogfish We also examine the utility of using spiny dogfish as a gelatinouszooplankton sampling device Using five calculation methodologies we provide bounds on potential abundance and biomassestimates of ctenophores in the Northeast US shelf ecosystemWe then contextualize these findings relative to the implications forthe Northeast US and any large marine ecosystem

1 Introduction

There have been several documented instances of gelatinouszooplankton blooms for a wide range of marine ecosystemsBoth enclosed (eg Black Sea Caspian Sea Sea of Azovand Sea of Marmara) and relatively enclosedsemiopen (egAdriatic Sea Baltic Sea Gulf of Mexico Bering Sea andMediterranean Sea) marine ecosystems have exhibited theseblooms [1ndash5] These increases in gelatinous zooplanktonabundance have been variously attributed to eutrophicationwater mass warming and overfishing [1ndash4 6ndash8] Theseincreases can also have significant negative ecosystem-wideimpacts (eg [9ndash11]) Yet often the impact of these bloomson ecosystem trophodynamics and energy flow is poorlyunderstood

Additionally sampling gelatinous zooplankton remains amajor challenge for biological oceanography [7 12] One wayto overcome sampling difficulties for gelatinous organismsis to utilize fish as an in situ sampling device Use offish stomach contents has become increasingly widespreadfor obtaining basic vital information on difficult-to-samplemarine organisms [13ndash15]

In a prior study [16] we used fish stomachs (spiny dogfishSqualus acanthias Linnaeus 1758) to serve as a proxy estimateof relative abundance for Ctenophora in the Northeast US(NEUS Figure 1) continental shelf ecosystem Our resultsfrom that work suggested that the relative occurrence ofCtenophora in spiny dogfish stomachs was increasing from1981 to 2000 and after examining several assumptionsour results implied that ctenophore abundance was greatlyincreasing in the Northeast US continental shelf ecosystemYet the scope (ie order of magnitude) of these and similarstomach-based estimates is rarely presented in terms ofabsolute abundance or biomass There need to be someprotocols to place bounds on estimates of abundance andbiomass of these gelatinous zooplankton blooms in generalbut particularly as sampled by fish

In our prior study [16] we did not attempt to scaleour estimates to total abundance We also did not evaluatehow energetically important Ctenophora may be to theirldquosamplerrdquo fish particularly with respect to other prey itemsThus the objectives of this study were to evaluate the relativeimportance of ctenophores as prey for spiny dogfish in terms

Hindawi Publishing CorporationInternational Journal of OceanographyVolume 2014 Article ID 851809 8 pageshttpdxdoiorg1011552014851809

2 International Journal of Oceanography

45∘N

40∘N

35∘N

75∘W 70

∘W 65∘W

MAB

SNE

GB

GM

Atlantic Ocean

Figure 1 Map of the study area the Northeast US (NEUS)continental shelf Common regions of Gulf ofMaine (GM) GeorgesBank (GB) Southern New England (SNE) and Middle AtlanticBight (MAB) are highlighted

of their energetic value and to provide bounds of probablemagnitudes of abundance for these ctenophores in theNEUSWe do so by using several simple feedingmodels with a rangeof assumptions Although there are short-term or localizedestimates of Ctenophora and other gelatinous zooplanktondensities (eg [10 17 18]) for regions of the NEUS ecosystemnone are synoptic at broad spatial and temporal scales Ourwork although based upon field data represents a modelingapproach to provide some sensitivity to the estimates wewere attempting to provide that are notably difficult usingclassical zooplankton approaches Addressing the lack ofgood abundance estimates for gelatinous zooplankton in thisway should provide a broader ecosystem context for thepotential impact of these and similar gelatinous zooplanktonblooms

2 Materials and Methods

21 Background The broad-scale long-term sampling pro-gram of stomach contents of fishes from the NortheastUS continental shelf ecosystem (Figure 1) serves directlyto identify changes in fish diets and indirectly to identifychanges in the underlying ecosystem [15 19 20]The standardNational Marine Fisheries Service (NMFS) Northeast Fish-eries Science Center (NEFSC) bottom trawl survey program

has been conducted annually since 1963 [21 22] Duringthese ongoing surveys food habits data are collected from avariety of species These multispecies surveys are designed tomonitor trends in abundance and distribution and to providesamples to study the ecology of the large number of fish andinvertebrate species inhabiting the region Azarovitz [21] andNEFC [22] provide a more detailed description of the surveyprogram

Although the program started in 1963 we focused on ourstudy on spiny dogfish stomachs (119899 = 43489) collected from1981 to 2000 throughout the entire range of theNortheast USshelf surveys (ie from Cape Hatteras NC to Nova ScotiaFigure 1) Across the four regions depicted in the survey theseasonally averaged abundance of spiny dogfish for the periodof 1996ndash2000 ranged from 33 to 56million dogfish per regionFull details of the food habits sampling and data are given inLink and Almeida [19] and are only summarized here withparticular respect to spiny dogfish During the period of thestudy (1981ndash2000) spiny dogfish stomachs were examinedand prey-identified at sea immediately after the catch wassorted on deck Thus concerns over the degradation of anygelatinous zooplankton due to the effects of preservation informalin or ethanol [9] or rapid digestion [23] are largelyunmerited Data on total stomach volume (01 cm3minimumresolution) prey composition () numbers and lengthswere collected shipboard In addition a conversion fromvolumetric measurement of prey (cm3) to mass (g) wasexecuted to obtain biomass estimates of the food consumedThe range of annual average consumption of ctenophores ingramswas 04 to 46 gwith the time series average of 21 gThesize of dogfish sampled ranged from juveniles (sim35ndash40) cm tolarge mature females (sim110 cm) but were predominately themedium size classes (50ndash80 cm)

Ctenophora were readily identifiable in the stomachsof spiny dogfish at sea upon macroscopic inspection bytheir obvious firm-gelatin constitution small and clear ball-like shape uniquely (relative to any other spiny dogfishprey) colored pinkish-gray masses and particularly the ctenerows Stomach contents identified as Ctenophora could havebeen Mnemiopsis leidyi Pleurobrachia pileus or Bolinopsisinfundibulum but it is beyond the scope of the presentwork to distinguish between them Even after partial diges-tion Ctenophora in spiny dogfish stomachs were identifi-able particularly the ctene Spiny dogfish do not masticateCtenophora rather Ctenophora are ingested as whole preyitems

The traditional method for monitoring zooplankton lev-els in the Northeast US shelf ecosystem has been plank-ton nets However plankton net surveys from 1977 to thepresent only record a very small number of observations ofctenophores (less than 2 of all tows taken)When comparedwith direct methods of sampling gelatinous zooplanktonin the marine environment (eg nets) stomach samplingmethods largely eliminated concerns of specimens breakingapart and becoming unidentifiable andor indistinguishable[7 12 24] Our modeling efforts used a range of digestiontimes from 025 hours to 24 hours since the digestion timeof ctenophores in spiny dogfish has not been experimentallydetermined to our knowledge

International Journal of Oceanography 3

Table 1 Energy density for common spiny dogfish (Squalus acan-thias) prey items

Prey kJg ReferenceCtenophoresmdashlower 038 [9 23]Ctenophoresmdashupper 084 [9 23]Pandalusshrimpmdashlower 488 [25]Pandalusshrimpmdashupper 952 [25]Amphipods 967 [25]Generalinvertebratesmdashlower 100 [25]Generalinvertebratesmdashupper 100 [25]Medusae 025 [25]Ctenophores 021 [25]Cephalopods 550 [25]Bivalves 154 [25]Gastropods 228 [25]Zooplankton 164 [25]Generalcrustaceansmdashlower 350 [25]Generalcrustaceansmdashupper 540 [25]Tunicates 040 [25]Fishmdashlower 400 [26ndash28]Fishmdashupper 700 [26ndash28]Forage fishmdashlower 100 [26ndash28] Hartman pers commForage fishmdashupper 200 [26ndash28] Hartman pers comm

22 Energetic Contribution to Diet The significance ofctenophores in the diet of spiny dogfish was explored interms of consumption energy density and diet composition(percentage of weight) relative to other prey typesThe caloricvalue of ctenophores is estimated to be between 90 and200 cal gminus1 wet weight (1 cal = 41868 J) [24] Energy densitiesfor other common spiny dogfish prey were taken from theliterature (Table 1)

The energetic contribution of common prey items forspiny dogfish including ctenophores was estimated by usinga simple product of percent diet composition energy densityand mean amount of total food consumed Additionally wemade calculations that also included the digestion rate of theprey item to estimate the energetic contribution of commonprey items while accounting for the different digestion ratesof prey body types

23 Biomass Estimates To place bounds on the estimatesof potential abundance and biomass of ctenophores in theNortheast US shelf ecosystem we employed five calcula-tion methodologies The estimates here refer to biomassover the total area of the Northeast US shelf ecosystem

(230000 km2) The five methodologies were a digestion timeapproach a consumption model approach simple frequencyof occurrence a swept volume model and a plankton netmethod

231 Digestion TimeMethod Biomass of ctenophores withinthe whole of the NEUS was estimated using the massof ctenophores in the stomachs of spiny dogfish and theestimated digestion time of ctenophores within spiny dogfishThe mass of ctenophores per year (119861ct) on the continentalshelf was estimated as a function of the average mass ofctenophores found in dogfish stomachs in grams (119878) theestimated digestion time of a ctenophore in a dogfish stomachin hours (119863 scaled to 24 and multiplied by the number ofdays in a year) and the number of dogfish on the shelf (119873dog)where

119861ct = ((119878

11986324

) sdot 365) sdot 119873dog (1)

The amount of ctenophores found in dogfish (119878) came fromstomach content sampling conducted on routine surveysdescribed above The number of dogfish present on the shelfecosystem was taken from stock assessment estimates fromthe Northeast Fisheries Science Center [29 general surveytechniques noted above] We use the minimum maximumand average abundance of spiny dogfish from these estimatesto bound the possible range (119873dog) To convert ctenophorebiomass (119861ct) into ctenophore abundance (119873ct) we assumedan average individual mass of 036 g per ctenophore [23]

232 Consumption Model Method The biomass of cteno-phores on the shelf was also estimated using a consump-tion model method [30 31] In this case the biomass ofctenophores per year was estimated as a function of theaverage mass of ctenophores found in dogfish stomachs ingrams (119878) and the evacuation rate of ctenophores throughdogfish (119864) where

1198611015840

ct = 119864 sdot 24 sdot 119878 (2)

The 24 is the number of hours in a day and the evacuationrate (119864) is defined as

119864 = 120572119890120573119879119901 (3)

where 120572 and 120573 are fitted coefficients [32] This equationrelates119864 to temperature determined by laboratory studies andthe literature [32] where 120573 is the slope found to be consistentbetween prey types and 120572 is the intercept that is dependenton the prey type For this study 120572 was set from 0002 to 08and 120573was fixed to 0115 119879

119901is the mean temperature specified

here as 145 C (cf [33])To scale to an annual total estimate 1198611015840ct wasmultiplied by

the minimum swept area estimate of dogfish (119873dog)

119861ct = 119873dog sdot 1198611015840

ct sdot 365 (4)

where 365 is the number of days per year To convertctenophore biomass (119861ct) into ctenophore abundance (119873ct)we assumed an average individual mass of 036 g perctenophore [23]


233 Simple Frequency of Occurrence in Dogfish Method Asimple method of estimating the biomass of ctenophores wasused to estimate ctenophore biomass (119861ct) as a function of thepercent frequency of occurrence of ctenophores in dogfishstomachs (119891) the number of dogfish on the continental shelf(119873dog) and the average mass of ctenophores found in thestomachs of dogfish (119878) where

119861ct = 119891 sdot 119873dog sdot 119878 (5)

To convert ctenophore biomass (119861ct) into ctenophore abun-dance (119873ct) we assumed an average individual mass of 036 gper ctenophore [23]

234 Swept Volume of Dogfish Method The swept volume ofa dogfish was defined as the product of the gape area and thetime anddistance a dogfish swimsper dayWe assumed a gapewidth of 3 cm 22 hours of feeding in a day and a swimmingvelocity of 1m sminus1 Observations of spiny dogfishmorphologyand swimming behavior were used to conservatively estimategape width and swimming speed The feeding time estimatewas made to allow some time spent on nonfeeding activities(2 hours)Using the gapewidth as a diameter and scaled to thedaily distance swum (product of speed and swimming time)the resulting swept volume (119881

119904) for a dogfish was 4072m3

The mass of ctenophores per dogfish per day (1198611015840ct- scaledby 24 for a daily estimate) could be estimated by using thisswept volume (119881

119904) the average mass of ctenophores found

in the stomachs of dogfish (119878) and the percent frequency ofoccurrence of ctenophores in dogfish stomachs (119891) where

1198611015840

ct = 119881119904 sdot 119878 sdot 119891 sdot 24 (6)

Using the volume of water (119881shelf) in each of the four regions(the Gulf of Maine (GoM) Georges Bank (GB) SouthernNew England (SNE) and the Middle Atlantic Bight (MAB))on the continental shelf the number of days per year andthe number of dogfish present in each region (119873dog-reg) thebiomass of ctenophores 119861ct could be calculated where

119861ct = 1198611015840

ct sdot 365 sdot 119881shelf sdot 119873dog-reg (7)

Estimates of water volume (m3) were calculated fromNEFSCestimates of area and average depth for each region Thenumbers of dogfish found in each region were also fromNEFSC survey estimates These were then integrated into atotal for the entire shelf To convert ctenophore biomass (119861ct)into ctenophore abundance (119873ct) we assumed an averageindividual mass of 036 g per ctenophore [23]

235 Plankton Net Method Prior ctenophore abundanceestimates for the NEUS shelf were estimated directly system-wide as part of the Energy Modeling and Analysis Exercise(EMAX) [34] Using data from plankton tows estimates ofaverage abundance and biomass of ctenophores for the entiretime period were calculated in each of the four regions ofthe continental shelf previously described [35] These towswere routine 60 cm 333mm mesh bongo tows from theNMFS EcoMon sampling program Seasonal variation was

0

1

2

3

Her

ring

Shrim

p

Squi

d

Oth

erfis

hes

Cten

o

Biva

lves

Mac

kere

l

Die

t of d

ogfis

h (k

J)

Figure 2 Energy density of selected common prey types scaled bydiet composition

0

1

2

3

Her

ring

Shrim

p

Squi

d

Oth

er

fishe

s

Mac

kere

l

Biva

lves

Cten

o

StandardLow digest time

High digest time

Die

t of d

ogfis

h (k

J)

Figure 3 Energy density of common prey items scaled for dietcomposition and digestion time

not accounted for in the model but EMAX [34] indicateshigher concentrations during the periods of May-June andSeptember-October Regionally in this data set the Mid-dle Atlantic Bight and Southern New England had higherconcentrations than Georges Bank and the Gulf of MaineThe area of each region was used to determine a weightedabundance of ctenophores whichwere then integrated for theentire shelf

3 Results

31 Energetics The energy density (KJ gminus1) of commonspiny dogfish prey including ctenophores indicated thatherring andmackerel had the highest energy density whereasctenophores had the lowest energy density (Table 1) Whenenergy density was scaled by diet composition small pelagicfishes such as herring mackerel and other fishes were thelargest energy contributors to spiny dogfish diet (Figure 2)

When digestion time was factored into the scaled energydensity calculations the relative significance of ctenophoresincreased Under the lowest digestion time ctenophorescontributed as much energy to the diet of spiny dogfishas mackerel but were still much lower than other fishes(Figure 3)

32 Biomass Estimates321 Digestion Time Method Considering a range of pos-sible digestion times for ctenophores in dogfish the mean


025 05 075 1 2 3 4 5 6 12 24Digestion time (hr)

1E + 11

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no

Min estimated dogfishAvg estimated dogfishMax estimated dogfish

Figure 4 Estimated number of ctenophores as a function ofctenophore digestion time (h) forminimummaximum and averagedogfish abundance estimates

estimated number of ctenophores in this continental shelfecosystem ranged from 81 times 1013 at the fastest digestiontime of 025 h to 85 times 1011 at the slowest digestion time of24 h (Figure 4) The different estimates for the number ofdogfish (minimum average or maximum) did not notablyimpact the total abundance estimates of ctenophores for anygiven digestion time results varied less than one half of anorder of magnitude Most estimates were similar across theabundance of spiny dogfish and given range of digestiontimes typically on the order of 1012 to 1013 The meanestimates of biomass ranged from 306 to approximately30000 thousandmetric tons again depending upon the timeof digestion and estimate of dogfish abundanceThemajorityof the biomass estimates ranged between 5000 and 15000thousand metric tons

322 Consumption Model Method Considering a rangeof digestibility coefficients (120572) for ctenophores the meanestimated number of ctenophores in this continental shelfecosystem ranged from 22 times 1010 given the lowest 120572 to 87 times1013 for the highest 120572 (Figure 5) Differences in the range ofdogfish abundance estimates similarly resulted in a differencein the ctenophore estimate of less than half an order ofmagnitude Most abundance estimates were on the order of1011 to 1012 ctenophores in the ecosystemThe mean biomassestimates ranged from 78 to approximately 31000 thousandmetric tons Again the minimum or maximum abundanceestimate of spiny dogfish used only changed the results by lessthan one half of an order of magnitude

323 Simple Frequency of Occurrence in Dogfish MethodWhen using the simple frequency of occurrence method themean number of ctenophores was 16 times 108 ranging from37 times 107 to 13 times 109 using the minimum and maximumestimates of dogfish abundance (Figure 6) The biomassestimates of ctenophores using this method were all notablyless than 01 thousand metric tons

00002 00004 0002 0004 004 04 08Digestibility coefficient

1E + 11

1E + 10

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no


Figure 5 Estimated number of ctenophores as a function ofdigestibility coefficient (120572) for minimum maximum and averagedogfish abundance estimates

Avg Min Max1E + 00

1E + 03

1E + 06

1E + 09

Num

ber o

f cte

noph

ores

Figure 6 Estimates of ctenophore abundance using the simplefrequency of occurrence in dogfish method Results presented forminimum maximum and average dogfish abundance estimates

324 Swept Volume of Dogfish Method There were an esti-mated 12times 1010 ctenophores per year in the entire continentalshelf ecosystemusing the swept volumemethodThe estimateof ctenophore biomass was 42 thousand MT from thismethod

325 Plankton Net Method Using the plankton net andassociated methodology described in EMAX there wereapproximately 83times 1013 ctenophores in the entire continentalshelf ecosystem This estimate was derived from the averagectenophore concentration (10mminus2) of 22 88 20 and 6 forthe Middle Atlantic Bight Southern New England GeorgesBank andGulf ofMaine regions respectivelyThe estimate oftotal ctenophore biomasswas approximately 30000 thousandMT

326 Comparison and Context Overall the five methodsfor determining the abundance of ctenophores spanned sixorders of magnitude with mean values ranging between


Digestion time

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

num

ber o

f cte

noph

ores

Consumptionmodel

00

03

06

09

12

15

1E +

1E +

1E +

1E +

1E +

1E +

(a)

Digestiontime

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

biom

ass o

f cte

noph

ores

Consumptionmodel

minus 02

00

02

1E +

1E +

1E +

1E

04

(1000

MT)

(b)Figure 7 Average number (a) and average biomass (b) of ctenophores (1000MT) as estimated from the different methods

108 and 1013 (Figure 7) Total mean biomass estimates werebetween 05 MT and 30000 thousand MT

4 Discussion

41 Energetic Contribution to Diet Ctenophores have a lowenergy density relative to other spiny dogfish prey such asmackerel herring shrimp and squid When the energy den-sities of individual prey items are scaled by diet compositionsmall pelagic fishes become the most energetically dominantcomponent of the spiny dogfish diet

Our results do indicate that faster digestion times forgelatinous zooplankton can increase the energetic impor-tance of ctenophores in dogfishWe calculated the diet-scaledenergetic importance (energy density) of ctenophores for arange of digestion rates from 025 h to 24 h Our estimatesindicatemore than a fivefold difference in energy contributedby ctenophores when digestion times range from even just075 to 4 h This range of digestion times is shorter thanother common prey items like mackerel While we do nothave empirical data for the digestion time of ctenophores inspiny dogfish we do have empirically derived digestion ratesof a tentaculate ctenophore Pleurobrachia bachei in chumsalmon Oncorhynchus keta of 1 h [23] While we recognizedifferences in relative stomach size and intestine lengthand expect differences in gut passage times between spinydogfish and chum salmon to our knowledge experimentallydetermined digestion rates for ctenophores in dogfish do notexist Using the empirical salmon data as a rough estimatefor the digestion time in spiny dogfish ctenophores mightcontribute as much energy as mackerel to the spiny dogfishdiet However the final conclusion is that even if we assume a1 h digestion time ctenophores are still a very low energy preyitem for spiny dogfish and other fishes that eat them relativetomost other prey items As stated in previous reviews futureexperiments to determine digestion rates would allow formore accurate determination of the energetic contribution ofctenophores in the diet of fishes [9 11]

We infer from these results that spiny dogfish feedon ctenophores in an opportunistic feeding mode eatingthem as encountered while swimming in the water columnThis implies that spiny dogfish neither select for nor avoidctenophores It may be that ctenophores serve as a supple-mentary food source allowing spiny dogfish tomaintain some

basic energy demands but it is unlikely that spiny dogfishglean a large portion of their bioenergetic demands solelyfrom ctenophores We suspect that this is generally true forother fishes that prey upon gelatinous zooplankton with afew exceptions (eg Stromateid fishes such as Stromateusbrasiliensis Fowler 1906 or Seriolella porosa Guichenot 1848that feed almost exclusively on ctenophores) [35] Yet thusfar there are no fishes known to consume solely pelagiccoelenterates as their only prey [11]

42 Biomass Estimates Ourmodel analyses and assumptionsimply a level of uncertainty in amount of ctenophoresconsumed by spiny dogfish in the NEUS on the range of sixorders of magnitude Abundance estimates were on the orderof 108 to 1013 individuals in the NEUS Estimates for biomasswere similarly quite widespread roughly ranging between 101and 105 thousand MT These estimates are quite variable andencompass quite a large range but do provide a reasonablebound of possible estimates of ctenophore abundance Thiswork in many ways represents a rudimentary sensitivityanalysis among different methods and serves to provide abound about the true ctenophore abundance outside ofwhich most estimates are likely to be ecologically unfeasible

Some key assumptions in the different methods we usedall merit further investigation Chief among them is theidentification ofmajor unknowns digestion time ctenophoreweight and true abundance of ldquosamplerrdquo fish Obviouslythere is a tradeoff among the methods used in terms of dataor parameter requirements and simplicity That most of ourestimates provided values of similar orders ofmagnitude addsconfidence to the range of estimates presented

Furthermore a recent study from Narragansett BayRhode Island USA reported concentrations of ctenophoresbetween 01mminus3 and 1000mminus3 [36] Using the rough volumeof Narragansett Bay this would be a total abundance fromapproximately 297 times 108 to approximately 297 times 1012 and abiomass between 0386 and 3859 thousandMT Similarly theSea of Azov experienced an explosion of Mnemiopsis leidyiranging from 32 to 106 g m3 [37] Using a rough estimatefor the volume of the Sea of Azov this density suggestsan approximate biomass between 156 times 104 and 518 times104 thousand MT Conversely estimates of Ctenophora andother gelatinous zooplankton densities (eg [10 17 18]) forregions of the NEUS ecosystem (eg Gulf of Maine Georges


Bank) can be higher than those presented here but noneof those are synoptic at broad spatial and temporal scalesneeded to appropriately estimate Ctenophora abundance forthe entire NEUS ecosystem But again calculated estimatesfrom these other studies and the other ecosystems notedabove are of the same magnitude as ours and confirmthat when ctenophore blooms occur they are roughly atthis level of density In short because the many differentapproacheswe used provide estimates on the samemagnitudeas other studies we have higher confidence that our moresimplistic modeling approaches have reasonably boundedthis estimation problem

Ctenophora and other gelatinous zooplankton are inher-ently difficult to sample and survey particularly at synoptictemporal and spatial scales [7 12]Themerits of using a novelsampling device fish stomachs have been discussed elsewhere[13ndash15] particularly for ctenophores [16] Providing somesense of scaling to a system-wide estimate and some sense ofbounding to those estimates is a useful outcome of this workThat we have been able to provide a set of reasonable boundsof abundance estimates is not trivial

The spiny dogfish appears to be a good sampler forctenophores that can support studies like this one Previousstudies [16 20] have shown that the diet composition ofCtenophora in the spiny dogfish has remained consistentand without a clear trend in the amount eaten suggesting arelative constancy in the factors that determine the amount ofctenophora they consume Further confidence is gained in thestability within the diet of the spiny dogfish during this studyperiod Levels of consumption of major functional groups ofprey (eg small forage fishes) have remained constant evenwhen certain species might fluctuate When all other factorsabout the changes in ctenophore occurrence in the spinydogfish are considered we are left with accepting that thesedata represent a good proxy for the change in ctenophoreabundance [16]

The amount of gelatinous zooplankton in the worldrsquosoceans remains a major question The examples from otherecosystems (eg [1ndash5]) suggest that there may be many moregelatinous zooplankton than we suspect The implications ofhaving high gelatinous zooplankton biomass in an ecosystemhave been well chronicled (eg [9ndash11]) and are mostly nega-tive While ctenophores were the focus of this study it shouldbe pointed out that according to NEFSC plankton surveydata Northeast US shelf ecosystem gelatinous zooplanktonincludes ctenophores siphonophores salps hydromedusaeand scyphomedusae Potential impacts vary by ecosystembut can include significant predation on fish eggs fishlarvae and heightened competition for zooplankton prey[11] Ctenophores depending on species might affect fishegg concentrations (M leidyi) or inter alia compete forzooplankton prey in the case of P pileus [11] Thus it hasbecome increasingly imperative that we develop methods toestimate and measure gelatinous zooplankton in situ on asynoptic scale The approaches we present here highlight afew possible ways to estimate the abundance and biomassand reasonably place bounds on those estimates for hard tosample gelatinous zooplankton

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

The authors thank the numerous staff at the NEFSC pastand present who have collected fish stomachs on the routinesurveys They also thank two anonymous reviewers for theirconstructive comments on earlier drafts of this paper

References

[1] J E Purcell W M Graham and H J C Dumont JellyfishBlooms Ecological and Societal Importance Proceedings of theInternational Conference on Jellyfish Blooms vol 451 Hydrobi-ologia 2001

[2] T A Shiganova Z A Mirzoyan E A Studenikina et al ldquoPop-ulation development of the invader ctenophore Mnemiopsisleidyi in the Black Sea and in other seas of the MediterraneanbasinrdquoMarine Biology vol 139 no 3 pp 431ndash445 2001

[3] R D Brodeur H Sugisaki and G L Hunt Jr ldquoIncreasesin jellyfish biomass in the Bering Sea implications for theecosystemrdquoMarine Ecology Progress Series vol 233 pp 89ndash1032002

[4] A C Gucu ldquoCan overfishing be responsible for the successfulestablishment of Mnemiopsis leidyi in the Black Seardquo Estuar-ine Coastal and Shelf Science vol 54 no 3 pp 439ndash451 2002

[5] M Bilio and U Niermann ldquoIs the comb jelly really to blame forit all Mnemiopsis leidyi and the ecological concerns about theCaspian Seardquo Marine Ecology Progress Series vol 269 pp 173ndash183 2004

[6] B K Sullivan D Van Keuren andM Clancy ldquoTiming and sizeof blooms of the ctenophore Mnemiopsis leidyi in relation totemperature in Narragansett Bay RIrdquo Hydrobiologia vol 451pp 113ndash120 2001

[7] T Weisse M-T Gomoiu U Scheffel and F BrodrechtldquoBiomass and size composition of the Comb Jelly Mnemiopsissp in the north-western Black Sea during spring 1997 andsummer 1995rdquo Estuarine Coastal and Shelf Science vol 54 no3 pp 423ndash437 2002

[8] J E Purcell ldquoClimate effects on formation of jellyfish andctenophore blooms a reviewrdquo Journal of the Marine BiologicalAssociation of the United Kingdom vol 85 no 3 pp 461ndash4762005

[9] M N Arai ldquoInteractions of fish and pelagic coelenteratesrdquoCanadian Journal of Zoology vol 66 no 9 pp 1913ndash1927 1988

[10] C E Mills ldquoMedusae siphonophores and ctenophores asplanktivorous predators in changing global ecosystemsrdquo ICESJournal of Marine Science vol 52 no 3-4 pp 575ndash581 1995

[11] J E Purcell and M N Arai ldquoInteractions of pelagic cnidariansand ctenophores with fish a reviewrdquoHydrobiologia vol 451 pp27ndash44 2001

[12] W M Hamner L P Madin A L Alldredge R W Gilmerand P P Hamner ldquoUnderwater observations of gelatinous zoo-plankton sampling problems feeding biology and behaviorrdquoLimnology and Oceanography vol 20 pp 907ndash917 1975

[13] L Fahrig G R Lilly and D S Miller ldquoPredator stomachsas sampling tools for prey distribution atlantic cod (Gadus


morhua) and capelin (Mallotus villosus)rdquo Canadian Journal ofFisheries and Aquatic Sciences vol 50 no 7 pp 1541ndash1547 1993

[14] C L J Frid and S J Hall ldquoInferring changes in North Seabenthos from fish stomach analysisrdquo Marine Ecology ProgressSeries vol 184 pp 183ndash188 1999

[15] J S Link ldquoUsing fish stomachs as samplers of the benthos inte-grating long-term and broad scalesrdquo Marine Ecology ProgressSeries vol 269 pp 265ndash275 2004

[16] J S Link and M D Ford ldquoWidespread and persistent increaseof Ctenophora in the continental shelf ecosystem off NE USArdquoMarine Ecology Progress Series vol 320 pp 153ndash159 2006

[17] L P Madin S M Bollens E Horgan et al ldquoVoraciousplanktonic hydroids unexpected predatory impact on a coastalmarine ecosystemrdquoDeep-Sea Research Part II Topical Studies inOceanography vol 43 no 7-8 pp 1823ndash1829 1996

[18] S R Avent S M Bollens M Butler E Horgan and RRountree ldquoPlanktonic hydroids onGeorges Bank ingestion andselection by predatory fishesrdquoDeep-Sea Research Part II TopicalStudies in Oceanography vol 48 no 1ndash3 pp 673ndash684 2001

[19] J S Link and F P Almeida An Overview and History ofthe Food Web Dynamics Program of the Northeast FisheriesScience Center NOAA Technical Memorandum NMFS-NE-159 Woods Hole Mass USA 2000

[20] J S Link J K T Brodziak S F Edwards et al ldquoMarineecosystem assessment in a fisheries management contextrdquoCanadian Journal of Fisheries and Aquatic Sciences vol 59 no9 pp 1429ndash1440 2002

[21] T R Azarovitz ldquoA brief historical review of the Woods HoleLaboratory trawl survey time series Bottom trawl surveysrdquoCanadian Special Publication of Fisheries and Aquatic Sciencesvol 58 pp 62ndash67 1981

[22] Northeast Fisheries Center An Evaluation of the Bottom TrawlSurvey Program of the Northeast Fisheries Center NOAATechnical Memorandum NMFS-FNEC-52 National MarineFisheries Service Woods Hole Mass USA 1988

[23] M N Arai D W Welch A L Dunsmuir M C Jacobs and AR Ladouceur ldquoDigestion of pelagic Ctenophora and Cnidariaby fishrdquo Canadian Journal of Fisheries and Aquatic Sciences vol60 no 7 pp 825ndash829 2003

[24] T G Bailey J J Torres M J Youngbluth and G P OwenldquoEffect of decompression on mesopelagic gelatinous zooplank-ton a comparison of in situ and shipboard measurements ofmetabolismrdquoMarine Ecology Progress Series vol 113 no 1-2 pp13ndash28 1994

[25] FW Steimle and R J Terranova ldquoEnergy equivalents ofmarineorganisms from the continental shelf of the temperate North-west Atlanticrdquo Journal of Northwest Atlantic Fishery Science vol6 pp 117ndash124 1985

[26] K J Hartman and S B Brandt ldquoEstimating energy density offishrdquo Transactions of the American Fisheries Society vol 124 no3 pp 347ndash355 1995

[27] J W Lawson A M Magalhaes and E H Miller ldquoImportantprey species of marine vertebrate predators in the northwestAtlantic proximate composition and energy densityrdquo MarineEcology Progress Series vol 164 pp 13ndash20 1998

[28] J Pedersen and J R G Hislop ldquoSeasonal variations in theenergy density of fishes in the North Seardquo Journal of FishBiology vol 59 no 2 pp 380ndash389 2001

[29] Northeast Fisheries Science Center 37th Northeast RegionalStock Assessment Workshop (37th SAW) Advisory ReportNortheast Fishery Science Center Reference Document 03-17

National Marine Fisheries Service Northeast Fisheries ScienceCenter Woods Hole Mass USA 2003

[30] D M Eggers ldquoFactors in interpreting data obtained by dielsampling of fish stomachsrdquo Journal of the Fisheries ResearchBoard of Canada vol 34 pp 290ndash294 1977

[31] J M Elliot and L Persson ldquoThe estimation of daily rates of foodconsumption for fishrdquo Journal of Animal Ecology vol 47 pp977ndash991 1978

[32] J S Link L P Garrison and F P Almeida ldquoEcological inter-actions between Elasmobranchs and groundfish species on theNortheastern US Continental Shelf I Evaluating PredationrdquoNorth American Journal of Fisheries Management vol 22 pp550ndash562 2002

[33] M H Taylor C Bascunan and J P Manning Description ofthe 2004Oceanographic Conditions on theNortheast ContinentalShelf Northeast Fishery Science Center Reference Document05-03 National Marine Fisheries Service Northeast FisheriesScience Center Woods Hole Mass USA 2005

[34] J S Link C A Griswold E T Methratta and J Gunnard EdsDocumentation for the Energy Modeling and Analysis EXercise(EMAX) Northeast Fisheries Science Center Reference Doc-ument 06-15 US Department of Commerce National MarineFisheries Service Woods Hole Mass USA 2006

[35] H W Mianzan N Mari B Prenski and F Sanchez ldquoFish pre-dation on neritic ctenophores from the Argentine continentalshelf a neglected food resourcerdquo Fisheries Research vol 27 no1ndash3 pp 69ndash79 1996

[36] J H Costello B K Sullivan D J Gifford D Van Keuren and LJ Sullivan ldquoSeasonal refugia shoreward thermal amplificationand metapopulation dynamics of the ctenophore Mnemiopsisleidyi in Narragansett Bay Rhode Islandrdquo Limnology andOceanography vol 51 no 4 pp 1819ndash1831 2006

[37] S P Volovik Z A Myrzoyan and G S Volovik ldquoMnemiopsisleidyi in the Azov Sea biology population dynamics impact tothe ecosystem andfisheriesrdquo inProceedings of the ICES StatutoryMeeting pp 1ndash69 CM Documents 1993

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ClimatologyJournal of

EcologyInternational Journal of


EarthquakesJournal of


Hindawi Publishing Corporationhttpwwwhindawicom

Applied ampEnvironmentalSoil Science

Volume 2014

Mining


Journal of

Hindawi Publishing Corporation httpwwwhindawicom Volume 2014

International Journal of

Geophysics

OceanographyInternational Journal of


Journal of Computational Environmental SciencesHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal ofPetroleum Engineering


GeochemistryHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

Atmospheric SciencesInternational Journal of


OceanographyHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in


MineralogyInternational Journal of


MeteorologyAdvances in

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Paleontology JournalHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

ScientificaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014


Geological ResearchJournal of


Geology Advances in


45∘N

40∘N

35∘N

75∘W 70

∘W 65∘W

MAB

SNE

GB

GM

Atlantic Ocean

Figure 1 Map of the study area the Northeast US (NEUS)continental shelf Common regions of Gulf ofMaine (GM) GeorgesBank (GB) Southern New England (SNE) and Middle AtlanticBight (MAB) are highlighted

of their energetic value and to provide bounds of probablemagnitudes of abundance for these ctenophores in theNEUSWe do so by using several simple feedingmodels with a rangeof assumptions Although there are short-term or localizedestimates of Ctenophora and other gelatinous zooplanktondensities (eg [10 17 18]) for regions of the NEUS ecosystemnone are synoptic at broad spatial and temporal scales Ourwork although based upon field data represents a modelingapproach to provide some sensitivity to the estimates wewere attempting to provide that are notably difficult usingclassical zooplankton approaches Addressing the lack ofgood abundance estimates for gelatinous zooplankton in thisway should provide a broader ecosystem context for thepotential impact of these and similar gelatinous zooplanktonblooms

2 Materials and Methods

21 Background The broad-scale long-term sampling pro-gram of stomach contents of fishes from the NortheastUS continental shelf ecosystem (Figure 1) serves directlyto identify changes in fish diets and indirectly to identifychanges in the underlying ecosystem [15 19 20]The standardNational Marine Fisheries Service (NMFS) Northeast Fish-eries Science Center (NEFSC) bottom trawl survey program

has been conducted annually since 1963 [21 22] Duringthese ongoing surveys food habits data are collected from avariety of species These multispecies surveys are designed tomonitor trends in abundance and distribution and to providesamples to study the ecology of the large number of fish andinvertebrate species inhabiting the region Azarovitz [21] andNEFC [22] provide a more detailed description of the surveyprogram

Although the program started in 1963 we focused on ourstudy on spiny dogfish stomachs (119899 = 43489) collected from1981 to 2000 throughout the entire range of theNortheast USshelf surveys (ie from Cape Hatteras NC to Nova ScotiaFigure 1) Across the four regions depicted in the survey theseasonally averaged abundance of spiny dogfish for the periodof 1996ndash2000 ranged from 33 to 56million dogfish per regionFull details of the food habits sampling and data are given inLink and Almeida [19] and are only summarized here withparticular respect to spiny dogfish During the period of thestudy (1981ndash2000) spiny dogfish stomachs were examinedand prey-identified at sea immediately after the catch wassorted on deck Thus concerns over the degradation of anygelatinous zooplankton due to the effects of preservation informalin or ethanol [9] or rapid digestion [23] are largelyunmerited Data on total stomach volume (01 cm3minimumresolution) prey composition () numbers and lengthswere collected shipboard In addition a conversion fromvolumetric measurement of prey (cm3) to mass (g) wasexecuted to obtain biomass estimates of the food consumedThe range of annual average consumption of ctenophores ingramswas 04 to 46 gwith the time series average of 21 gThesize of dogfish sampled ranged from juveniles (sim35ndash40) cm tolarge mature females (sim110 cm) but were predominately themedium size classes (50ndash80 cm)

Ctenophora were readily identifiable in the stomachsof spiny dogfish at sea upon macroscopic inspection bytheir obvious firm-gelatin constitution small and clear ball-like shape uniquely (relative to any other spiny dogfishprey) colored pinkish-gray masses and particularly the ctenerows Stomach contents identified as Ctenophora could havebeen Mnemiopsis leidyi Pleurobrachia pileus or Bolinopsisinfundibulum but it is beyond the scope of the presentwork to distinguish between them Even after partial diges-tion Ctenophora in spiny dogfish stomachs were identifi-able particularly the ctene Spiny dogfish do not masticateCtenophora rather Ctenophora are ingested as whole preyitems

The traditional method for monitoring zooplankton lev-els in the Northeast US shelf ecosystem has been plank-ton nets However plankton net surveys from 1977 to thepresent only record a very small number of observations ofctenophores (less than 2 of all tows taken)When comparedwith direct methods of sampling gelatinous zooplanktonin the marine environment (eg nets) stomach samplingmethods largely eliminated concerns of specimens breakingapart and becoming unidentifiable andor indistinguishable[7 12 24] Our modeling efforts used a range of digestiontimes from 025 hours to 24 hours since the digestion timeof ctenophores in spiny dogfish has not been experimentallydetermined to our knowledge









119861ct = ((119878

11986324

) sdot 365) sdot 119873dog (1)



1198611015840

ct = 119864 sdot 24 sdot 119878 (2)


119864 = 120572119890120573119879119901 (3)





119861ct = 119873dog sdot 1198611015840

ct sdot 365 (4)




119861ct = 119891 sdot 119873dog sdot 119878 (5)







1198611015840

ct = 119881119904 sdot 119878 sdot 119891 sdot 24 (6)


119861ct = 1198611015840




0

1

2

3

Her

ring

Shrim

p

Squi

d

Oth

erfis

hes

Cten

o

Biva

lves

Mac

kere

l

Die

t of d

ogfis

h (k

J)


0

1

2

3

Her

ring

Shrim

p

Squi

d

Oth

er

fishe

s

Mac

kere

l

Biva

lves

Cten

o


High digest time

Die

t of d

ogfis

h (k

J)



3 Results






1E + 11

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no







1E + 11

1E + 10

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no



Avg Min Max1E + 00

1E + 03

1E + 06

1E + 09

Num

ber o

f cte

noph

ores






Digestion time

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

num

ber o

f cte

noph

ores

Consumptionmodel

00

03

06

09

12

15

1E +

1E +

1E +

1E +

1E +

1E +

(a)

Digestiontime

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

biom

ass o

f cte

noph

ores

Consumptionmodel

minus 02

00

02

1E +

1E +

1E +

1E

04

(1000

MT)



4 Discussion















Acknowledgments


References


















































Volume 2014

Mining


Journal of



Geophysics







Journal of




Advances in











Geology Advances in









119861ct = ((119878

11986324

) sdot 365) sdot 119873dog (1)



1198611015840

ct = 119864 sdot 24 sdot 119878 (2)


119864 = 120572119890120573119879119901 (3)





119861ct = 119873dog sdot 1198611015840

ct sdot 365 (4)




119861ct = 119891 sdot 119873dog sdot 119878 (5)







1198611015840

ct = 119881119904 sdot 119878 sdot 119891 sdot 24 (6)


119861ct = 1198611015840




0

1

2

3

Her

ring

Shrim

p

Squi

d

Oth

erfis

hes

Cten

o

Biva

lves

Mac

kere

l

Die

t of d

ogfis

h (k

J)


0

1

2

3

Her

ring

Shrim

p

Squi

d

Oth

er

fishe

s

Mac

kere

l

Biva

lves

Cten

o


High digest time

Die

t of d

ogfis

h (k

J)



3 Results






1E + 11

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no







1E + 11

1E + 10

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no



Avg Min Max1E + 00

1E + 03

1E + 06

1E + 09

Num

ber o

f cte

noph

ores






Digestion time

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

num

ber o

f cte

noph

ores

Consumptionmodel

00

03

06

09

12

15

1E +

1E +

1E +

1E +

1E +

1E +

(a)

Digestiontime

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

biom

ass o

f cte

noph

ores

Consumptionmodel

minus 02

00

02

1E +

1E +

1E +

1E

04

(1000

MT)



4 Discussion















Acknowledgments


References


















































Volume 2014

Mining


Journal of



Geophysics







Journal of




Advances in











Geology Advances in



119861ct = 119891 sdot 119873dog sdot 119878 (5)







1198611015840

ct = 119881119904 sdot 119878 sdot 119891 sdot 24 (6)


119861ct = 1198611015840




0

1

2

3

Her

ring

Shrim

p

Squi

d

Oth

erfis

hes

Cten

o

Biva

lves

Mac

kere

l

Die

t of d

ogfis

h (k

J)


0

1

2

3

Her

ring

Shrim

p

Squi

d

Oth

er

fishe

s

Mac

kere

l

Biva

lves

Cten

o


High digest time

Die

t of d

ogfis

h (k

J)



3 Results






1E + 11

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no







1E + 11

1E + 10

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no



Avg Min Max1E + 00

1E + 03

1E + 06

1E + 09

Num

ber o

f cte

noph

ores






Digestion time

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

num

ber o

f cte

noph

ores

Consumptionmodel

00

03

06

09

12

15

1E +

1E +

1E +

1E +

1E +

1E +

(a)

Digestiontime

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

biom

ass o

f cte

noph

ores

Consumptionmodel

minus 02

00

02

1E +

1E +

1E +

1E

04

(1000

MT)



4 Discussion















Acknowledgments


References


















































Volume 2014

Mining


Journal of



Geophysics







Journal of




Advances in











Geology Advances in



1E + 11

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no







1E + 11

1E + 10

1E + 12

1E + 13

1E + 14

1E + 15

Estim

ated

num

ber o

f cte

no



Avg Min Max1E + 00

1E + 03

1E + 06

1E + 09

Num

ber o

f cte

noph

ores






Digestion time

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

num

ber o

f cte

noph

ores

Consumptionmodel

00

03

06

09

12

15

1E +

1E +

1E +

1E +

1E +

1E +

(a)

Digestiontime

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

biom

ass o

f cte

noph

ores

Consumptionmodel

minus 02

00

02

1E +

1E +

1E +

1E

04

(1000

MT)



4 Discussion















Acknowledgments


References


















































Volume 2014

Mining


Journal of



Geophysics







Journal of




Advances in











Geology Advances in


Digestion time

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

num

ber o

f cte

noph

ores

Consumptionmodel

00

03

06

09

12

15

1E +

1E +

1E +

1E +

1E +

1E +

(a)

Digestiontime

model

Simplefrequency

Dogfish sweptarea

Plankton net

Avg

biom

ass o

f cte

noph

ores

Consumptionmodel

minus 02

00

02

1E +

1E +

1E +

1E

04

(1000

MT)



4 Discussion















Acknowledgments


References


















































Volume 2014

Mining


Journal of



Geophysics







Journal of




Advances in











Geology Advances in








Acknowledgments


References


















































Volume 2014

Mining


Journal of



Geophysics







Journal of




Advances in











Geology Advances in





































Volume 2014

Mining


Journal of



Geophysics







Journal of




Advances in











Geology Advances in