Assessment of trophic dynamics of cephalopods and large pelagic fishes in the central North Atlantic Ocean using stable isotope analysis

Deep-Sea Research II 95 (2013) 63–73

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Assessment of trophic dynamics of cephalopods and large pelagic fishes in the central North Atlantic Ocean using stable isotope analysis John M. Logan a,b,n, Molly E. Lutcavage c a

Large Pelagics Research Center, Department of Biological Sciences, University of New Hampshire, Durham, NH 03824, USA Massachusetts Division of Marine Fisheries, 1213 Purchase Street, New Bedford, MA 02740, USA c Large Pelagics Research Center, Department of Environmental Conservation, University of Massachusetts Amherst, Marine Station, PO Box 3188, Gloucester, MA 01931 USA b

a r t i c l e i n f o

abstract

Available online 20 July 2012

Pelagic ecosystems in the central North Atlantic Ocean support numerous commercially-exploited tuna, shark, and billfish species, which rely largely on cephalopod as well as fish and crustacean prey. Carbon and nitrogen stable isotope analyses were performed on tuna and billfish predators as well as cephalopod prey species sampled during two research longline cruises (2001–02) to study their trophic structure. Nitrogen stable isotope (d15N) analyses revealed similarity in trophic position (TP) among sampled fish predator species, with large swordfish occupying the highest TP. Species with wider vertical distributions (swordfish and bigeye tuna) had higher d15N values than species more constrained to the epipelagic zone (yellowfin tuna and dolphinfish). Analysis of tissue nitrogen isotope values showed an ontogenetic increase for swordfish and white marlin but no effects for other sampled fish species. For cephalopods as a group, d15N increased with size. Smaller cephalopods sampled in this study had d15N values that were about one TP below co-occurring tunas and billfishes, confirming their importance as a prey resource. Larger cephalopods had similar d15N values to tunas and billfishes, indicating that these large cephalopods occupy a comparable TP to their fish predators. Both carbon and nitrogen stable isotope values of large pelagic fishes showed spatial gradients relative to conspecifics analyzed in coastal regions, which can be used to trace large scale movements. Published by Elsevier Ltd.

Keywords: Cephalopods Food webs Nitrogen Swordfish Trophic structure Tuna fisheries

1. Introduction Despite being harvested for decades in commercially valuable fisheries, the trophic relationships of tunas, sharks, and billfishes in the central North Atlantic Ocean are not well understood. Along with toothed cetaceans, these species occupy top trophic niches (Bowman et al., 2000; Dragovich, 1969; Kitchell et al., 2006) and range widely across pelagic habitats in search of prey (Gunn and Block, 2001; Kohler et al., 1998; Ortiz et al., 2003; Sharp, 2001). Commercial fishery removals (Hinke et al., 2004; Kitchell et al., 2002) and climate variability (Alheit, 2009) presumably impact trophic structure in pelagic ecosystems by altering top down and bottom up flows, while shifts in distribution and composition of mid-trophic level prey may alter that of their predators (Polovina, 1996). To predict impacts of these various influences on top predators, existing trophic structure must first be understood (Maury and Lehodey, 2005). Until recently, analysis of stomach contents via direct sampling was the only method of describing

n Corresponding author at: Massachusetts Division of Marine Fisheries, 1213 Purchase Street, New Bedford, MA 02740, USA. Tel.: þ1 508 990 2860x141; fax: þ1 508 990 0449. E-mail address: [email protected] (J.M. Logan).

0967-0645/$ - see front matter Published by Elsevier Ltd. http://dx.doi.org/10.1016/j.dsr2.2012.07.013

pelagic food webs, but its limitations are significant (Chipps and Garvey, 2007), especially when compared to the large spatial and temporal foraging scales of highly mobile species of tunas and billfishes (e.g., Galuardi et al., 2010; Neilson et al., 2009). Recently, stomach content analysis identified ommastrephid squids and other cephalopods as important prey for large pelagic fishes in the central North Atlantic (Logan et al., 2013), consistent with their central diet role for marine mammals, sea birds, and fishes in pelagic ecosystems worldwide (Boyle and Rodhouse, 2005a; Clarke, 1996; Croxall and Prince, 1996; Smale, 1996). While the importance of cephalopods as a prey group is well documented, the diet and trophic status of cephalopods themselves are not well understood (Rodhouse and Nigmatullin, 1996). Stable isotope analysis has been used to study the trophic ecology of large pelagic fishes (e.g., Estrada et al., 2003; Me´nard et al., 2007; Revill et al., 2009) and cephalopods (e.g., Cherel et al., 2009a, 2009b; Ruiz-Cooley et al., 2004). Isotope values reflect average assimilated diet over a range of timescales, dictated by growth and turnover rates for a given tissue or compound (Gannes et al., 1998). Cephalopod beaks, which accumulate in predator stomachs, show particular promise for dietary reconstruction by stable isotope analysis (Cherel and Hobson, 2005; Jackson et al., 2007). Whole beaks, beak wing material (Hobson and Cherel,

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2006), and mantle tissue (Stowasser et al., 2006) reflect recent diet (last life history phase). In comparison, in fishes, isotope ratios in liver and white muscle reflect dietary information over timescales of weeks and months (Logan et al., 2006; MacNeil et al., 2006; Suzuki et al., 2005). Carbon stable isotope ratios (13C/12C; d13C) increase moderately between diet and consumer (Sweeting et al., 2007a) and provide a chemical record of primary production sources even at higher trophic levels (Fry, 2006). Nitrogen stable isotope ratio (15N/14N; d15N) increases are generally more amplified ( 2.5–3.5% for fish and cephalopod muscle (Hobson and Cherel, 2006; Sweeting et al., 2007b; Vanderklift and Ponsard, 2003)) and can be used as a proxy for trophic position (TP) when combined with estimates of baseline isotope values and diet-tissue discrimination factors (Post, 2002). In a companion paper (Logan et al., 2013), we reported stomach content results from exploratory longline cruises undertaken in the central North Atlantic to establish the biological and reproductive status of Atlantic bluefin tuna (ABFT) and other large pelagic fish species (Lutcavage and Luckhurst, 2001). These research cruises intercepted top fish predators in the important transition region between the Gulf Stream boundary current, the north Sargasso Sea, and continental shelf. Here we report on carbon and nitrogen stable isotope analyses performed on fish liver and muscle tissue as well as cephalopod beak and mantle material collected from stomachs of sampled fishes. Values were compared among species and families and across sizes to assess community trophic structure. Cephalopod isotope data were compared to the pelagic fish predators from which they were sampled to evaluate the relative trophic position of cephalopods in these offshore food webs.

2. Methods 2.1. Sample collection Liver and dorsal white muscle samples were collected (Table 1) from fish captured during directed longline research cruises to the central North Atlantic Ocean in 2001 and 2002 (See Logan et al. (2013) for a detailed description of methods). Longline sets were made from 351N–431N from June–July, 2001 and 231N–36oN from May–June, 2002, and samples for stable isotope analysis (SIA) were collected from a latitudinal range from 34 to 431N (Fig. 1). Cephalopod beaks and mantle tissue were collected from stomach contents of these pelagic fish predators (Table 2). Fish liver and muscle samples and whole stomachs were stored frozen prior to analysis. Cephalopod beaks obtained from stomach contents were then transferred to 70% ethanol while mantle subsamples were re-frozen. Cephalopod beaks and mantle material were identified to the family level based on morphological characteristics (Clarke, 1986;

Maddison and Schulz, 2007). Cephalopod mantle length (ML) was estimated based on beak lower rostral length (LRL) (Clarke, 1962, 1980; Pe´rez-Ga´ndaras, 1983; Wolff, 1984). For cephalopod beaks, lateral wings were used for most samples. For the smallest beaks, the whole lower beak was analyzed.

2.2. Stable isotope analysis In preparation for analysis, liver, white muscle, mantle, and beak samples were lightly rinsed with deionized water and dried in glass scintillation vials at 60 1C for at least 48 h. Samples were then homogenized using a Mixer/Mills (SPEX SamplePrep, LLC Metuchen, NJ, USA) with stainless steel vials (soft tissues) or mortar and pestle (beaks). Aliquots of homogenized sample (0.6–1.2 mg) were packed into 4  6 mm tin cups and analyzed for d13C, d15N, % carbon, and % nitrogen by continuous flow using a Costech ECS4010 elemental analyzer (Costech Analytical Technologies, Inc, Valencia, CA, USA) coupled with a DELTAplus XP isotope ratio mass spectrometer (Thermo Scientific, Bremen, Germany) at the University of New Hampshire Stable Isotope Laboratory (UNH). Smaller beak samples for which material was limited were analyzed under high amplification using sample masses of 0.1–0.8 mg. All carbon and nitrogen isotope data are reported in d notation according to the following equation:   Rsample dX ¼ 1  1000 Rs tan dard where X is 13C or 15N and R is the ratio 13C/12C or 15N/14N (Peterson and Fry, 1987). Standard materials are Vienna Pee Dee belemnite (VPDB) for carbon and atmospheric N2 (AIR) for nitrogen. Analytical precision is  0.2% for d13C and d15N. All d13C and d15N values were normalized on the VPDB and AIR scales with IAEA CH6 (10.4%), CH7 ( 31.8%), N1 (0.4%) and N2 (20.3%). All liver and muscle d13C samples were corrected for lipid content using a mass balance equation (Fry, 2002) with parameters specific to Atlantic bluefin tuna (Thunnus thynnus) liver and white muscle (Logan et al., 2008). Mantle d13C samples were corrected with parameters based on a general dataset of fish muscle (Logan et al., 2008). While our parameters matched the appropriate tissue type, they were not species-specific and likely induced some error in d13C estimates (Logan et al., 2008). Lipid content was minimal for muscle tissue from all species except swordfish, but liver values were elevated and likely influenced modeled estimates (Table 3). Cephalopod beak d15N samples were corrected for chitin content using a mass balance equation (Fry, 2002), with estimates for protein C:N of 3 and protein–chitin d15N discrimination of 9% (Macko et al., 1990; Schimmelmann and DeNiro, 1988; Webb et al., 1998).

Table 1 Summary of samples of white muscle and liver (in parentheses) collected for stable isotope analysis. Sizes are fork length (cm) 7 SD. Location values are minimum and maxium latitude sampling sites rounded to the nearest degree. NA refers to cases where no samples were collected. Species

Albacore tuna (Thunnus alalunga) Bigeye tuna (Thunnus obesus) Blue marlin (Makaira nigricans) Dolphinfish (Coryphaena hippurus) Swordfish (Xiphias gladius) White marlin (Tetrapturus albidus) Yellowfin tuna (Thunnus albacares)

2001

2002

n

Length (cm)

Location (1N)

n

Length (cm)

Location (1N)

59 27 0 10 63 4 36

96 7 6 91 7 22 NA 95 7 13 148 7 26 161 7 14 132 7 19

34–43 35–43 NA 41–43 34–43 34–36 34–43

5 (4) 3 (1) 2 0 18 (6) 21 (3) 16 (10)

1007 7 (99 7 7) 887 32 (123) 2027 44 NA 154 740 (159 7 41) 162 7 9 (162 7 1) 116 737 (115 740)

34–37 36–37 37–43 NA 34–37 34–37 35–37

(36–37) (37)

(35–37) (36) (35–37)

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65

Fig. 1. Map of fish collection locations for 2001 and 2002.

Table 2 Sample collection summary of cephalopod tissues analyzed for d13C and d15N. All samples were obtained from stomach contents of large pelagic fish predators. Family

Tissue

Predator

Architeuthidae Chiroteuthidae Cycloteuthidae Gonatidae Histioteuthidae Octopoda Ommastrephidae Onychoteuthidae Vampyroteuthidae Histioteuthidae Architeuthidae Ommastrephidae

Beak Beak Beak Beak Beak Beak Beak Beak Beak Mantle Mantle Mantle

Yellowfin tuna (1), Yellowfin tuna (1), Dolphinfish (1) Swordfish (2) Yellowfin tuna (2), Yellowfin tuna (1), Yellowfin tuna (2), Swordfish (4) Swordfish (1) Bigeye tuna (1) Swordfish (1) Yellowfin tuna (1),

Swordfish (4) Swordfish (1), Albacore tuna (2)

Swordfish (3), Albacore tuna (5), Bigeye tuna (1), Dolphinfish (1) Swordfish (1), Albacore tuna (2) Swordfish (16), Albacore tuna (2), Bigeye tuna (2), Longbill spearfish (1)

Bigeye tuna (1), Longbill spearfish (1), Swordfish (8)

2.3. Statistical analyses Cluster analyses using Ward’s minimum variance were performed on mean d13C and d15N data for the pelagic fish liver and muscle datasets as well as the cephalopod beak dataset to visualize isotopic groupings. To examine size-based dynamics in trophic position, effects of the length of individuals and latitude of capture location on nitrogen stable isotope values were explored using multiple linear regression. Analyses were performed for liver and muscle samples from swordfish (Xiphias gladius) and yellowfin tuna (Thunnus albacares) as well as muscle samples of

Mantle length (mm)

Latitude (1N)

13.2–314.8 42.7–106.2 162 156.4–372.4 0.8–140.2 9.4–80.6 70.9–651.9 155.0–410.6 35.3 80.0 285 120–406

32–37 29–37 34 34–35 28–37 30–37 28–37 34–35 37 33 32 29–37

albacore tuna (Thunnus alalunga), bigeye tuna (Thunnus obesus), white marlin (Tetrapturus albidus), and dolphinfish (Coryphaena hippurus). Analyses were also performed for ommastrephid mantle samples and pooled cephalopod beak samples. Latitude was included as a parameter to control for potential spatial effects on tissue isotope values due to regional baseline shifts (Hobson, 1999). For cases where length effects were not statistically significant for fish species, further analyses were performed to assess statistical power (Galva´n et al., 2010). Blue marlin (Makaira nigricans) were excluded from regression analyses due to limited sample size (Table 1).

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Table 3 Mean7 SD d13C, d15N, C:N, and trophic position (TP) values for liver and muscle from large pelagic fishes and squids. Species

Liver

Albacore tuna Bigeye tuna Swordfish (All) Swordfish (r 150 cm FL) Swordfish (4150 cm FL) White marlin Yellowfin tuna Blue marlin Dolphinfish Ommastrephidae

Muscle

d13C (%)

d15N (%)

C:N

TP

d13C (%)

d15N (%)

C:N

TP

 18.4 7 0.3  17.9  17.2 7 0.4  17.9  17.0 70.2  17.8 7 0.3  17.6 7 0.5 – – –

7.67 0.7 8.5 9.87 0.4 9.1 10.07 0.3 8.57 0.7 8.07 0.5 – – –

4.2 70.2 4.0 5.9 71.7 5.6 6.07 1.9 5.5 72.1 4.07 0.3 – – –

4.87 0.5 5.5 6.57 0.3 5.9 6.67 0.2 5.57 0.5 5.17 0.4 – – –

 17.5 70.4  16.8 70.3  16.6 70.5  16.6 70.6  16.5 70.4  16.7 70.3  17.1 70.3  16.5 70.8  16.9 70.5  17.4 70.4

10.17 0.4 10.37 0.7 10.87 0.6 10.67 0.6 11.1 7 0.4 10.07 1.3 9.67 0.6 10.37 0.0 9.97 0.6 9.77 1.1

3.1 7 0.0 3.2 7 0.1 4.4 7 1.9 4.0 7 1.7 4.9 7 2.1 3.2 7 0.2 3.1 7 0.1 3.2 7 0.1 3.1 7 0.0 3.3 7 0.2

4.77 0.3 4.87 0.4 4.97 0.3 4.87 0.3 5.17 0.3 4.97 0.6 4.57 0.3 4.87 0.3 4.37 0.3 4.77 0.5

Trophic positions were estimated based on d15N of muscle and liver samples using the equation: TP ¼ l þ

d15 Nsecondary consumer d15 Nbase Dn

(Post, 2002), where secondary consumer is the pelagic fish or squid, base is a lower trophic level reference organism, l is the TP of the reference organism, and Dn is the diet-tissue discrimination factor for d15N. Published copepod data from the study region (Graham et al., 2009; Montoya et al., 1992) were used to estimate base d15N using mean values of 4% and 5% for samples collected below and above 411N, respectively. Separate baseline values were used to account for a higher d15N baseline for northern samples collected near the shelf edge (Graham et al., 2009). Copepods were assigned a l (TP) value of 2.0, and Dn was assumed to be 2.1% and 1.3% for muscle and liver, respectively, based on estimates for yellowfin tuna (Graham, 2008). Calculations were made for each individual sample, then average and SD estimates were generated for each pelagic predator. All analyses were performed using the program R (R Development Core Team, 2008). All values are reported as mean7one standard deviation (SD) unless otherwise noted.

3. Results Mean isotope values for all fish species combined were  17.07 0.5% and 10.270.8% (muscle; n¼264) as well as 17.770.5% and 8.570.9% (liver; n¼24) for carbon and nitrogen, respectively (Fig. 2). Based on muscle data, pelagic fishes formed two main groups, with swordfish separated from remaining species. Liver isotope data grouped species into two trophic guilds, with large swordfish (4150 cm FL) separated from small swordfish and remaining species (Fig. 2). Albacore tuna had the lowest mean d13C values for both muscle (17.5%) and liver ( 18.4%) while blue marlin ( 16.5%) and swordfish ( 17.2%) had the highest values for muscle and liver, respectively. For d15N, yellowfin tuna (muscle: 9.6%) and albacore tuna (liver: 7.6%) had the lowest values while swordfish had the highest values for both muscle (10.8%) and liver (9.8%; Fig. 2). Trophic position estimates based on liver samples were higher and more variable than muscle-based estimates (Table 3). For muscle, TP estimates were similar for all pelagic fishes as well as ommastrephid squids, with all mean estimates between 4.3 (dolphinfish) and 5.1 (large swordfish). Liver estimates were more variable, ranging from 4.8 for albacore tuna to 6.6 for large swordfish. Tissue d15N values increased significantly with size for swordfish liver and muscle and white marlin muscle, but not for any other species (Fig. 3; Table 4). Statistical power varied among individual tests, with minimum detectable d15N shift varying

from 0.8% (yellowfin tuna muscle) to 4.2% (dolphinfish muscle; Table 5). Isotope values were determined for both mantle and beak wing material from one architeuthid and four individual ommastrephid prey samples. For d15N, the mean7SD difference between mantle and chitin-corrected beak material was 4.270.3%. For d13C, the difference was  0.670.4%. These values are similar to previous estimates (Cherel and Hobson, 2005; Cherel et al., 2009a; Hobson and Cherel, 2006; Ruiz-Cooley et al., 2006). Considerable isotopic overlap existed among cephalopod families, with high intra-family variability in both isotope ratios (Fig. 4). Chiroteuthidae had the highest intra-family variability due to a single squid (106.272.9 mm ML) that had a d13C value  2% and d15N value  5% higher than samples from smaller individuals (45.673.2 mm ML, n¼3). Despite intra-family variability, individual families generally grouped into two isotope guilds based on d13C differences with Octopoda, Histioteuthidae, and Chiroteuthidae having lower values than the remaining families (Fig. 4). While Chiroteuthidae values were variable, Octopoda and Histioteuthidae formed the lowest trophic level guild with both the lowest mean d13C and d15N, Ommastrephidae and Architeuthidae represented the second grouping, Vampyroteuthidae, Cycloteuthidae and Onychoteuthidae made up the third group, and Gonatidae had the highest mean d15N value among all families (Fig. 4). When all beak samples were analyzed as a single dataset, d15N increased significantly with mantle length (p ¼0.0009, r2 ¼0.1946). Ommastrephidae was the most prevalent prey group in large pelagic fish stomach contents (Logan et al., 2013) and had isotope ranges for mantle samples of  18.3 to  17.0% for d13C and 7.5– 10.6% for d15N (n¼9). Ommastrephid beak samples ranged from  19.4 to 16.0% for d13C and 1.5–7.8% for d15N (n ¼20). Three ommastrephid beak samples and one mantle sample were outliers and were excluded from analyses, because they were likely longline bait rather than natural prey (Fig. 4). These samples had mean7SD values of  18.870.5% (d13C) 15 15 and 15.070.8% (d N), after adjusting beak d N values for an estimated 4.2% increase. Mantle from Illex spp. (Ommastrephidae) sampled from a commercial longline bait supplier had similar values of  18.370.4% and 13.4 70.3% (n¼3).

4. Discussion 4.1. Trophic structure of cephalopods and large pelagic fishes Large pelagic fishes and cephalopods had a high degree of overlap in isotope values although subtle isotope groupings were evident. Dolphinfish and yellowfin tuna occupied the lowest TP among pelagic fishes based on muscle data while albacore tuna,

J.M. Logan, M.E. Lutcavage / Deep-Sea Research II 95 (2013) 63–73

12 Albacore tuna Bigeye tuna Blue marlin Dolphinfish Small Swordfish Large Swordfish White marlin Yellowfin tuna

10

Albacore tuna Bigeye tuna Small Swordfish Large Swordfish White marlin Yellowfin tuna

10 δ15N

δ15N

12

67

8

8

6 −18

−17

−16

−15

−19

−18

−17

−16

δ13C

0.03

0.06

0.02

0.04

Height

Height

δ13C

0.01

0.02

Yellowfin.tuna

Albacore.tuna

White.marlin

Bigeye.tuna

Small.Swordfish

Large.Swordfish

White.marlin

Dolphinfish

Yellowfin.tuna

Albacore.tuna

Blue.marlin

Bigeye.tuna

Large.swordfish

Small.swordfish

0.00

Fig. 2. Mean 7SD carbon and nitrogen isotope values (%) and cluster analyses based on these mean values from muscle (A,B) and liver (C,D) samples from large pelagic fishes. Small and large swordfish correspond to individuals r150 and 4 150 cm fork length, respectively.

bigeye tuna, white marlin, blue marlin, ommastrephid squid, and small swordfish made up an intermediate TP. Large swordfish had the highest TP of sampled species. This was mirrored by swordfish stomach contents sampled during the cruise, which also contained the largest prey, including a diversity of cephalopod species (Logan et al., 2013). Albacore tuna had the lowest liver carbon and nitrogen isotope values and also consumed the smallest prey, including a higher proportion of crustaceans (Logan et al., 2013). Bigeye tuna and swordfish, which have a wide vertical range (Carey and Robison, 1981; Schaefer and Fuller, 2002), had higher d15N values than the more epipelagic yellowfin tuna and dolphinfish (Brill et al., 1999; Palko et al., 1982). Yellowfin tuna and dolphinfish diet from this region contains a variety of small Sargassumassociated fishes including the families Exocoetidae, Diodontidae, Molidae, and Monacanthidae (Logan et al., 2013), which could account for slightly lower d15N values for these pelagic predators. Stable isotope analyses were not performed on any shark species that we or others sampled in this region, but shortfin mako sharks (Isurus oxyrinchus) prey on swordfish (Bowman et al., 2000) and have higher d15N values than co-occurring tunas and billfishes in pelagic food webs in the Pacific (Revill et al., 2009). Atlantic bluefin tuna were not collected during the surveys, but are known to frequent this region from tagging (Galuardi et al., 2010; Walli et al., 2009) and catch data (Miyabe and Hiramatsu, 1994). Historical feeding studies from the central North Atlantic revealed a diet of fishes of the family Bramidae as well as ommastrephid squids and octopods (Matthews et al., 1977). Estimates of TP using isotope data are sensitive to a variety of factors and should be used with caution. Assumptions include

tissue isotopic steady state with local food webs, consistent trophic discrimination factors among species, relatively stable baseline isotope values, and constrained movements within the timescales of tissue turnover. Complete isotopic turnover likely requires several months for tuna white muscle (Graham, 2008), during which time predators could migrate both vertically and horizontally to feed on prey associated with varied isotopic baselines. Trophic discrimination factors are poorly validated for large pelagic fishes and likely vary among species, diet types, and environmental conditions (Barnes et al., 2007; Sweeting et al., 2007a, 2007b). Estimates of TP are highly sensitive to trophic discrimination estimates (Post, 2002), and the high and variable TP estimates from liver tissue are likely due to the presumed low discrimination factor for this tissue type. Individuals of the same size class of different cephalopod families generally share similar isotope values, but size alone did not account for observed trophic relationships. For example, a small chiroteuthid squid had a d15N value greater than Atlantic cephalopods more than twice its size (e.g., Onychoteuthidae), and chiroteuthids also had higher d15N values than larger cephalopods in other oceans (Cherel and Hobson, 2005; Cherel et al., 2009b; Revill et al., 2009). Relatively large gonatids had the highest mean d15N values, consistent with previous stomach content studies (Nixon, 1987). These inter-family isotope differences could also be related to isotope baseline differences (Takai et al., 2000). For example, high-latitude gonatid squids found near the Grand Banks would have a higher baseline d15N value than cephalopods inhabiting more tropical regions (Graham et al., 2009). Isotopic differences have also been detected among species

J.M. Logan, M.E. Lutcavage / Deep-Sea Research II 95 (2013) 63–73

200

250

50

100 150 Length (cm)

200

0

δ15N 0

50

100 150 Length (cm)

200

250

50

100 150 Length (cm)

200

50

100 150 Length (cm)

200

50

100 150 Length (cm)

200

250

0

50

100 150 Length (cm)

200

250

0

50

100 150 Length (cm)

200

250

0

50

100 150 Length (cm)

200

250

14 13 12 11 10 9 8 7 6

250

14 13 12 11 10 9 8 7 6 0

14 13 12 11 10 9 8 7 6

250

14 13 12 11 10 9 8 7 6

250

14 13 12 11 10 9 8 7 6

δ15N 0

δ15N

100 150 Length (cm)

14 13 12 11 10 9 8 7 6 0

δ15N

50

δ15N

δ15N

0

14 13 12 11 10 9 8 7 6

δ15N

14 13 12 11 10 9 8 7 6

δ15N

δ15N

68

14 13 12 11 10 9 8 7 6

Fig. 3. Nitrogen isotope values (%) for muscle from (A) swordfish, (B) yellowfin tuna, (C) albacore tuna, (D) bigeye tuna, (E) dolphinfish, (F) white marlin, (G) all fish muscle samples, and liver from (H) swordfish and (I) yellowfin tuna relative to fork length (cm).

Table 4 Multiple linear regression slope, intercept, and p-values for liver and muscle d15N values. Species

n

Slope 7 SE

P-value Length

Liver Swordfish Yellowfin tuna

6 10

0.026n 0.956

Muscle Albacore tuna Bigeye tuna Dolphinfish Swordfish White marlin Yellowfin tuna All samples

64 30 10 81 25 52 264

0.360 0.119 0.175 o 0.001n o 0.001n 0.195 o 0.001n

Latitude

0.096 0.727 0.251 0.090 0.003n 0.232 o 0.001n 0.009n 0.003n

Length

Latitude

0.0167 0.004 0.000 7 0.004

0.350 7 0.146 0.093 7 0.256

 0.0107 0.011 0.0097 0.006 0.0167 0.011 0.0127 0.002 0.0717 0.016 0.0047 0.003 0.0087 0.001

0.023 7 0.020 0.096 7 0.054 1.250 7 0.281 0.020 7 0.017  0.711 7 0.147 0.081 7 0.030 0.043 7 0.014

Intercept 7SE

 5.178 7 5.693 4.672 7 9.232 10.244 7 1.553 5.629 7 2.013  44.3777 12.272 8.255 7 0.749 24.096 7 5.831 5.940 7 1.118 7.550 7 0.579

The ‘‘All samples’’ dataset refers to the complete collection of muscle data, including blue marlin. n

Significant relationship between nitrogen isotope value and length or latitude (Po 0.05).

from a common family (Parry, 2008), and our results could include multiple species because samples were only identified to family level. Following adjustment for d15N differences between beak and mantle tissue, most smaller cephalopods were one TP below the

fishes that had consumed them (assuming trophic increases of  2.3%), while larger cephalopods occupied a similar TP relative to fish predators. Although ommastrephids occupy a TP below most tunas, billfishes, and sharks, the largest have d15N values similar to fish predators (Revill et al., 2009), and in some cases even a slightly

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higher average TP. With highly adapted physical and sensory capabilities, large squids can hunt a broad spectrum of prey across a wide depth range (Amaratunga, 1983; Boyle and Rodhouse,

2005b). Squid families Ommastrephidae, Enoploteuthidae, Histioteuthidae, and Onychoteuthidae exploit prey from the surface to41000 m (Rosa et al., 2008), a range matched regularly by bigeye tuna (T. obesus), swordfish (X. gladius), and bluefin tuna (T. thynnus) (Block et al., 2001; Carey and Robison, 1981; Schaefer and Fuller, 2002; Takahashi et al., 2003). In the North Atlantic, isotopic evidence confirms that large cephalopods share a common TP with teleost as well as marine mammal predators (Cherel et al., 2009b). Preservation in ethanol results in slight decreases (0.2%) and increases (þ0.6%) for d13C and d15N, respectively, in ommastrephid beaks (Ruiz-Cooley et al., 2011). Comparisons of undigested prey with stomach contents have shown both no effect (Grey et al., 2002) and increases in both d13C and d15N (Guelinckx et al., 2008) for fish stomach contents. Since beak and mantle samples from our study were obtained from stomach contents and beaks were stored in ethanol, cephalopod TP estimates could be somewhat positively biased relative to large pelagic fishes, which were collected fresh and stored frozen.

Table 5 Statistical power of d15N-based assessments of changes in trophic position (TP) with size. Lmax refers to the maximum recorded size for a given species. DTP indicates the relative TP shifts detectable under different discrimination factor estimates. Species

n

Muscle Albacore tuna Bigeye tuna Dolphinfish Yellowfin tuna

Size range

64 30 10 52

83–112 60–134 75–123 59–160

Lmax

140 250 210 239

Detectable d15N shift (%)

1.32 1.48 4.16 0.76

DTP 2.1%

3.2%

0.63 0.70 1.98 0.36

0.41 0.46 1.30 0.24

DTP

10

59–154

239

2.36

1.3%

2.0%

4.2. Size and d15N

1.82

1.18

Cephalopod isotope values generally increased with size for individuals within a family. Increases in d15N with size have been

15 p = 0.0143 r2 = 0.4456

0.2 0.15 0.1 0.05

δ15N

Onychoteuthidae

Cycloteuthidae

Vampyroteuthidae

Gonatidae

Ommastrephidae

Architeuthidae

Histioteuthidae

Chiroteuthidae

5

0 0

10

10 15 Lower rostral length (mm)

GO CY CH

6

OM HI

10

VA ON AR

Bait Natural Prey

p = 0.0110 r2 = 0.8435

5

OC

4

20

δ15N

δ15N

5

15

8

2

0 −20

−19

−18

−17

−16

δ13C 15

AR CH CY

p = 0.0020 r2 = 0.2639

0

100

200

300

400

Mantle length (mm) GO HI OC

OM ON VA

δ15N

10

Bait Natural Prey

10 Octopoda

Height

Liver Yellowfin tuna

69

5

0 0

5

10 15 Lower rostral length (mm)

20

Fig. 4. Cephalopod isotope data (%) showing (A) cluster analysis based on mean beak isotope values, (B) mean 7 SD carbon and nitrogen isotope values for beak samples of Architeuthidae (AR), Chiroteuthidae (CH), Cycloteuthidae (CY), Gonatidae (GO), Histioteuthidae (HI), Ommastrephidae (OM), Onychoteuthidae (ON), and Vampyroteuthidae (VA), (C) nitrogen isotope values relative to beak lower rostral length (LRL) for the same families listed in (B), (D) ommastrephid beak nitrogen isotope values relative to LRL, and e) ommastrephid mantle nitrogen isotope values relative to mantle length. For (D) and (E), values are identified as suspected natural prey and suspected longline gear bait.

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observed in subantarctic cephalopods (Cherel and Hobson, 2005), and for ommastrephids sampled in the Pacific (Parry, 2008; Ruiz-Cooley et al., 2006) and Indian oceans (Cherel et al., 2009a). Most pelagic cephalopods are generalists that consume proportions of crustaceans, fishes, and other cephalopods in response to availability (Amaratunga, 1983; Nixon, 1987), and ommastrephids, like many cephalopod families, are cannibalistic (Boyle and Rodhouse, 2005b) to an increasing level with size (Nixon, 1987). Observed increases in isotope values with size are likely a result of a dietary shift from crustaceans to cephalopods and fishes (Amaratunga, 1983; Boyle and Rodhouse, 2005b; Summers, 1983). Nitrogen isotope values increased with size for swordfish but not for any tuna species. Ontogenetic increases in isotope values have also been observed for swordfish in the Indian (Me´nard et al., 2007) and Pacific oceans (Revill et al., 2009; Young et al., 2006), consistent with stomach content data showing a positive relationship between swordfish and prey length (Logan et al., 2013). Results showing no nitrogen isotopic changes with size agree with past isotope analyses for yellowfin tuna in the Indian Ocean (Me´nard et al., 2007), but do not reflect observed increases in prey size from stomach content data (Logan et al., 2013). Differences between stomach content and isotope results could be due to differences in timescales, with gut evacuation estimated at o24 h (Olson and Boggs, 1986) and isotope turnover requiring weeks (liver) to months (white muscle) for yellowfin tuna (Graham, 2008). Rapid digestion of smaller, lower trophic level prey (Olson and Boggs, 1986) would also influence stomach content but not isotope results. Ontogenetic shifts in both diet and tissue d15N values were detected for yellowfin tuna near the Hawaiian islands (Graham et al., 2007), but for smaller size classes than those analyzed in our study. Albacore muscle d15N values increased with fork length in the ˜ i et al., 2011), but Northeast Atlantic and Mediterranean Sea (Gon decreased with size in the Pacific Ocean (Revill et al., 2009). While not significant, the slope of the best fit regression line relating albacore length to muscle d15N in our study was negative, suggesting a similar trend to that observed in the Pacific for albacore in pelagic ecosystems (Revill et al., 2009). The lack of a significant relationship between tissue d15N values and fish size for albacore and other species may be partly due to insufficient statistical power from our limited sample size and size range. For example, dolphinfish d15N changes would have needed to exceed 4% to be detected with the existing dataset. In white marlin, increases in d15N with size could reflect ontogenetic changes in TP, but bias associated with spatial baseline shifts is more likely. No changes in prey size were observed with size of white marlin sampled in the tropical central Atlantic (Vaske et al., 2004). The variation in d15N (8.8–13.0%) that we observed across a smaller size range of individuals (144–186 cm) would correspond to an increase of more than a trophic position (Sweeting et al., 2007b). While d15N generally increases more than d13C with trophic level, for a d15N increase reflective of more than one trophic position, d13C should increase by 1–2% (Sweeting et al., 2007a). An additional multiple regression for d13C revealed a significant negative relationship (p¼0.009, slope¼  0.01470.005). We sampled white marlin from a relatively narrow latitudinal range, but spatial bias could still impact isotope values due to the relatively slow turnover rates of fish muscle (Hesslein et al., 1993) and the highly migratory nature of this species (Ortiz et al., 2003). 4.3. Isotopes and fish movement We note that dispersal across areas with differing isotopic baselines could have influenced isotope values and TP estimates for the pelagic fishes sampled. For example, we observed spatial

trends with sampling location for muscle nitrogen isotopes of dolphinfish and yellowfin tuna, but not swordfish, albacore, or bigeye tuna. Latitudinal increases in muscle d15N for yellowfin tuna and dolphinfish agree with latitudinal trends for zooplankton (Graham et al., 2009) and likely reflect diminishing influence of N2 fixation, which is most prevalent in the Caribbean and Sargasso Sea region (Karl et al., 2002), south of the longline sampling transects. While latitudinal effects were not detected for other species, isotope values could reflect a blend of isotopic baselines across migratory pathways. For example, electronic tagging indicates that within a few months, movements of individual swordfish span the northern and southern sampling regions of this study, including 15N-depleted waters of the Caribbean Sea (Neilson et al., 2009). Inclusion of tissues with more rapid turnover (MacNeil et al., 2005) and compound-specific analyses (Popp et al., 2007) should help to reduce potential spatial biases in future studies. Large pelagic fishes from the central North Atlantic had higher d13C and lower d15N values than conspecifics from coastal regions (Das et al., 2000; Estrada et al., 2005), likely due to different nitrogen (Altabet, 1988; Karl et al., 2002; Montoya et al., 2002; Owens, 1987) and primary production sources (Rooker et al., 2006) in coastal and pelagic regions. These isotope gradients between distant foraging grounds are being used to track migrations between coastal and offshore regions through SIA in other oceans (Graham et al., 2009) and could be similarly applied to the North Atlantic.

4.4. Suitability of cephalopod beaks for trophic studies Isotopic analysis of beaks has the potential to delineate cephalopod trophic ecology (Cherel and Hobson, 2005), but there are a number of caveats. Beaks are composed mainly of chitin and protein, which have different d15N values (Schimmelmann and DeNiro, 1988). We addressed this by normalizing all of the d15N values based on literature estimates of protein–chitin isotope discrimination and protein C:N from non-cephalopod sources. Similar parameters used in normalization equations for d13C for lipids significantly differ among tissue types and species (Logan et al., 2008), and relationships between chitin and protein probably vary. Future isotope analyses of beaks should either include chemical chitin extractions (Schimmelmann and DeNiro, 1988) or mathematical corrections using parameters based on cephalopod beak and mantle samples. While beaks are valuable for isotope analysis (Cherel and Hobson, 2005), they can persist in stomachs for a long time (Van Heezik and Seddon, 1989). A highly mobile predator may transport beaks across distant regions with different isotope base˜a et al., 1985) that could confound lines (Clarke, 1972; Galva´n-Magan isotope results. Despite some limitations, stable isotopes and complementary chemical tracers can be used to interpret and expand upon stomach content analysis and ecosystem modeling approaches ˜ez and Keyl, 2010; Jackson et al., 2007; in diet studies, (Iba´n Semmens et al., 2007). Consequently, this will lead to increased understanding of the trophic ecology and movements of this important class of organisms.

4.5. Applications and future research Estimates of absolute and relative trophic position as well as size-based isotopic patterns can be used in future food web modeling studies for the central North Atlantic. Further sampling of cephalopods as well as other mid-trophic level species would complement our existing dataset. Compound specific isotope analyses would also better separate trophic and migratory

J.M. Logan, M.E. Lutcavage / Deep-Sea Research II 95 (2013) 63–73

influences on predator isotope values, which are becoming more explicitly understood through the application of electronic tagging (Neilson et al., 2009). Ecosystem modeling in the Pacific has addressed potential impacts of commercial fishery removals (Hinke et al., 2004) as well as climate change (Griffiths et al., 2010) on open ocean food webs. Isotope data from our study combined with stomach content and other biological data would facilitate such efforts for the North Atlantic.

Acknowledgments We thank Central North Atlantic Steering Committee members Brian Luckhurst, John Lamkin, Ziro Suzuki, William Richards, Richard Brill and Scott Heppell (Chief Scientist, 2001); Michael Musyl (Chief Scientist, 2002); Lisa Natanson, Steven G. Wilson, David Murphy, Mike Cox and Richard Gorham; Captains Carvel Eisenhauer of F/V Hamilton Banker and Hubert Kearley of F/V Atlantic Optimist, Captains John Caldwell, Scott Drabinowicz (F/V Eagle Eye II), and their crews; Clearwater Fine Foods, Don Aldous, (Canadian Bluefin Research Fund); Philip Ryan and Andy Henneberry (IVY Fisheries). We are grateful to Sarah McLaughlin for cruise management, and Anne Everly for data analysis, Mitch Roffer (Roffs, Inc.) and Don Olson (RSMAS) for oceanographic forecasting, and the late Peter C. Wilson. We thank Dan O’Brien, John Barnes and the government of Bermuda for assistance with cruises and quota administration, and the National Research Institute of Far Seas Research, Japan. We would also like to thank Rebecca Toppin and Sean Smith for their assistance with cephalopod beak identification, Andrew Ouimette and the staff of the University of New Hampshire Stable Isotope Laboratory for assistance with stable isotope analyses, Ben Galuardi for assistance with figure preparation, Sarah Bean, Rebecca Toppin, and two anonymous reviewers for providing helpful comments on earlier drafts of this manuscript, and David Galva´n for helpful input on statistical power analyses. This work was supported by NOAA grant # NA16FM2840 to M. Lutcavage and the Canadian Bluefin Tuna Research Fund and Fisheries and Oceans Canada. This paper is a contribution to a CLIOTOP initiative to develop understanding of squid in pelagic ecosystems. References Alheit, J., 2009. Consequences of regime shifts for marine food webs. Int. J. Earth Sci. 98, 261–268. Altabet, M.A., 1988. Variations in nitrogen isotopic composition between sinking and suspended particles-implications for nitrogen cycling and particle transformation in the open ocean. Deep Sea Res. 35 (4), 535–554. Amaratunga, T., 1983. The role of cephalopods in the marine ecosystem. In: Caddy, J.F. (Ed.), Advances in Assessment of World Cephalopod Resources. FAO Fish. Tech. Pap. FAO, Rome, pp. 379–415. Barnes, C., Sweeting, C.J., Jennings, S., Barry, J.T., Polunin, N.V.C., 2007. Effect of temperature and ration size on carbon and nitrogen stable isotope trophic fractionation. Funct. Ecol. 21 (2), 356–362. Block, B.A., Dewar, H., Blackwell, S.B., Williams, T.D., Prince, E.D., Farwell, C.J., Boustany, A., Teo, S.L.H., Seitz, A., Walli, A., Fudge, D., 2001. Migratory movements, depth preferences, and thermal biology of Atlantic bluefin tuna. Science 293 (5533), 1310–1314. Bowman, R.E., Stillwell, C.E., Michaels, W.L., Grosslein, M.D., 2000. Food of Northwest Atlantic Fishes and Two Common Species of Squid. NOAA Technical Memorandum NMFS-NE-155. 138 pp. Boyle, P., Rodhouse, P., 2005a. Cephalopods as prey. In: Boyle, P., Rodhouse, P. (Eds.), Cephalopods-Ecology and Fisheries. Blackwell Publishing, Oxford, pp. 234–258. Boyle, P., Rodhouse, P., 2005b. Cephalopods as predators. In: Boyle, P., Rodhouse, P. (Eds.), Cephalopods-Ecology and Fisheries. Blackwell Publishing, Oxford, pp. 222–233. Brill, R.W., Block, B.A., Boggs, C.H., Bigelow, K.A., Freund, E.V., Marcinek, D.J., 1999. Horizontal movements and depth distribution of large adult yellowfin tuna (Thunnus albacares) near the Hawaiian Islands, recorded using ultrasonic telemetry: implications for the physiological ecology of pelagic fishes. Mar. Biol. 133 (3), 395–408.

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