CONTRIBUTION OF CEPHALOPOD PREY TO THE DIET OF LARGE PELAGIC FISH PREDATORS IN THE CENTRAL NORTH ATLANTIC OCEAN MITSG 13-34

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1 CONTRIBUTION OF CEPHALOPOD PREY TO THE DIET OF LARGE PELAGIC FISH PREDATORS IN THE CENTRAL NORTH ATLANTIC OCEAN J. Logan, R. Toppin et al. MITSG Sea Grant College Program Massachusetts Institute of Technology Cambridge, Massachusetts NOAA Grant No. NA11OAR Project No E/E-66-NSI Reprinted from Deep Sea Research Part II: Topical Studies in Oceanography 95: 74 82, October 2013.

2 Deep-Sea Research II 95 (2013) Contents lists available at ScienceDirect Deep-Sea Research II journal homepage: Contribution of cephalopod prey to the diet of large pelagic fish predators in the central North Atlantic Ocean John M. Logan a,b,n, Rebecca Toppin a, Sean Smith c, Benjamin Galuardi a,d, Julie Porter e, Molly Lutcavage a,d a Large Pelagics Research Center, Department of Biological Sciences, University of New Hampshire, Durham, NH 03824, USA b Massachusetts Division of Marine Fisheries, 1213 Purchase Street, New Bedford, MA 02740, USA c Bedford Institute of Oceanography, Fisheries and Oceans Canada, 1 Challenger Drive, P.O. Box 1006, Dartmouth, NS, Canada B2Y 4A2 d Large Pelagics Research Center, Department of Environmental Conservation, University of Massachusetts Amherst, Marine Station, P.O. Box 3188, Gloucester, MA 01931, USA e St. Andrews Biological Station, Fisheries and Oceans Canada, St. Andrews, NB, Canada E5B2L9 article info Available online 28 June 2012 Keywords: Cephalopods Food webs Ommastrephid Stomach content Swordfish Trophic structure Tuna fisheries abstract Trophic studies documenting the importance of cephalopod prey for large pelagic fish predators have been performed recently for open ocean ecosystems in the Pacific and Indian oceans, but similar data for the central North Atlantic Ocean have been lacking. A series of longline sampling cruises targeting large pelagic fish species was undertaken in the central North Atlantic Ocean in , and stomach samples were analyzed from a variety of tuna, shark, and billfish species to help fill this data gap. Stomach samples were collected from nine species (n¼170 non-empty stomachs), with the majority of stomachs from Atlantic swordfish (Xiphias gladius; n¼69), yellowfin tuna (Thunnus albacares; n¼31), and albacore tuna (Thunnus alalunga; n¼28). Ommastrephid squids were the most ubiquitous prey group across predator species and sampling years. Secondary cephalopod prey included octopods, histioteuthids, and architeuthids. Mesopelagic fishes and Sargassum-associated fishes were also identified as important prey. Diet composition varied spatially and prey size increased with predator size for swordfish and yellowfin tuna. Our results support findings in other ocean basins that demonstrate the importance of squid to large pelagic fishes and highlight the need for more research on their ecological and biophysical dynamics. Published by Elsevier Ltd. 1. Introduction Cephalopods are common prey for marine mammals, sea birds, and various large pelagic fishes in pelagic ecosystems worldwide (Boyle and Rodhouse, 2005; Clarke, 1996; Croxall and Prince, 1996; Smale, 1996). Cephalopods grow rapidly with high food conversion rates and provide an important link in open ocean food webs worldwide between lower trophic levels and higher trophic level fishes (Boucher-Rodoni et al., 1987; Nigmatullin, 2002; O Dor and Wells, 1987). Recent studies have demonstrated the importance of cephalopods in the diets of tunas, sharks, dolphinfishes, and billfishes in pelagic ecosystems throughout the Pacific Ocean (e.g., Markaida and Hochberg, 2005; Olson and Galván-Magaña, 2002; Olson et al., 2010; Preti et al., 2012; Young et al., 2006; Young et al., 2010). Tuna and billfish diet in the Indian Ocean has also recently been shown to contain high proportions n Corresponding author at: Massachusetts Division of Marine Fisheries, New Bedford, MA 02740, USA. Tel.: þ x141; fax: þ address: john.logan@state.ma.us (J.M. Logan). of cephalopod prey (e.g., Potier et al., 2007; Rohit et al., 2010). Recent food web studies of offshore ecosystems in the tropical central Atlantic Ocean have shown cephalopods to be primary or secondary prey for tunas and billfishes (Cherel et al., 2007; Liming and Liuxiong, 2004; Sabatié et al., 2003). While studies of open ocean food webs have been performed recently for the tropical Atlantic and other oceans, surprisingly little work has been conducted on fish predators in the North Atlantic Ocean. Historical diet studies have shown cephalopods to be important prey for a variety of tunas (Matthews et al., 1977), dolphinfish (Gibbs and Collette, 1959), and swordfish (Stillwell and Kohler, 1985) in the central North Atlantic and Gulf Stream margins. Directed studies of cephalopod communities have been performed for the North Atlantic using pelagic trawls and submersibles (Gartner et al., 2008; Vecchione and Roper, 1991; Vecchione and Pohle, 2002), but without complementary predator prey studies. More recent diet data needed to compare food web dynamics of the central North Atlantic with other ocean basins are largely lacking. In 2001 and 2002, exploratory longline cruises were undertaken in the central North Atlantic to establish the biological and /$ - see front matter Published by Elsevier Ltd.

3 J.M. Logan et al. / Deep-Sea Research II 95 (2013) reproductive status of large pelagic species in this region, with additional legs conducted primarily in more equatorial areas (Satoh et al., 2004). These research cruises intercepted large pelagic fishes in the important transition region between the Gulf Stream boundary current, the north Sargasso Sea, and continental shelf. Here we report on the food habits of tunas, billfishes, and sharks examined during these cruises, with a focus on cephalopod prey. We relate cephalopod prey composition to historical studies from the central North Atlantic as well as more recent studies from other oceans. 2. Material and methods 2.1. Sample collection Longline sets extended from 351N to 431N in June July, 2001 and from 231N to 361N in May June, 2002 (Fig. 1). In 2001, stomachs were sampled by the F/V Hamilton Banker, which made 16 longline sets (17,880 hooks) of approximately 74 km each, in two different areas. Sets 1 7 occurred in a thermally stratified area near the New England Sea Mounts, while sets 8 16 took place near the Tail of the Grand Banks of Newfoundland, a slightly cooler region with more surface mixing. F/V Eagle Eye II made 29 longline sets (21,000 hooks) between May 6 and June 30, 2002 extending from the New England Sea Mounts south towards the Caribbean Sea (Fig. 1) Stomach content analysis Stomach samples were collected from albacore tuna (Thunnus alalunga), bigeye tuna (Thunnus obesus), yellowfin tuna (Thunnus albacares), dolphinfish (Coryphaena hippurus), blue marlin (Makaira nigricans), white marlin (Tetrapturus albidus), longbill spearfish (Tetrapturus pfluegeri), swordfish (Xiphias gladius), and shortfin mako (Isurus oxyrinchus; Table 1). Stomachs were removed at sea and stored frozen. Samples were later thawed and weighed to the nearest gram, opened, and their contents were washed over a 1000 mm sieve. Contents were preserved in 70% ethanol for later measurement, weighing, and identification. Empty stomachs were not included in analyses since fish may evacuate their guts during capture (Chase, 2002). Samples were identified to the lowest possible taxonomic classification. Whole prey were measured to the nearest cm and each prey group was weighed g. We based prey identification on comparisons with field guides and online keys (Campana, 2004; Carpenter, 2002; Clarke, 1986; Maddison and Schulz, 2007; Robins and Ray, 1986; Scott and Scott, 1988). We identified cephalopods mainly based on funnel locking apparatus (FLA) and beak morphology. Since beaks are believed to accumulate in marine predator stomachs with minimal digestion (Hernández-Garcia, 1995; Van Heezik and Seddon, 1989), we analyzed loose beaks separately from remaining prey fractions. A total of 450 lower beaks were obtained from all stomach samples with 78 and 372 beaks found in 2001 and 2002 samples, respectively. Prey length and wet weight were estimated using existing regression equations for otolith length (Smale et al., 1995) and beak lower rostral length (LRL), respectively (Clarke, 1962, 1980; Pérez-Gándaras, 1983; Wolff, 1984). We evaluated the accuracy of mantle length estimates based on beak measurements by comparing them with measured whole mantle samples from the same individuals for families Architeuthidae, Histioteuthidae, and Ommastrephidae (n¼17) Statistical analysis We determined sample size adequacy by generating cumulative prey curves for each predator species for each sampling year. Cumulative prey curves estimate the diversity of prey species observed across increasing sample sizes (Ferry and Caillet, 1996). For a given predator species, bootstrapping techniques were used to generate 500 random stomach samples of a given sample size. Unique prey types were assigned based on the lowest level of identification for a given prey group, which typically corresponded to the family level. Any prey identified more coarsely (e.g., cephalopoda vs. Ommastrephidae) were not included as unique prey. To test for adequacy of sample size, the slope across the final four points of each prey curve was compared to a slope of zero using a Student s t-test (Bizzarro et al., 2007). We grouped stomach contents by % weight and % occurrence for each individual stomach and calculated them for each predator Fig. 1. Map of longline set locations for 2001 and Dashed lines indicate the general area sampled by a previous survey of large pelagic fish diet (Matthews et al., 1977).

4 76 J.M. Logan et al. / Deep-Sea Research II 95 (2013) Table 1 Summary of samples collected for stomach content analysis. Sample sizes are reported for non-empty stomachs, with number of empty stomachs listed in parentheses. Sizes are fork length (cm)7sd. Location values are minimum and maximum latitude sampling sites rounded to the nearest degree. Species Total n Size (cm) Location (1N) n Size (cm) Location (1N) n Size (cm) Location (1N) Albacore tuna (Thunnus alalunga) 18 (6) (2) (8) Bigeye tuna (Thunnus obesus) 8 (3) (3) Blue marlin (Makaira nigricans) Dolphinfish (Coryphaena hippurus) Longbill spearfish (Tetrapturus 0 3 (1) (1) pfluegeri) Shortfin mako (Isurus oxyrinchus) Swordfish (Xiphias gladius) 24 (5) (2) (7) White marlin (Tetrapturus albidus) Yellowfin tuna (Thunnus albacares) Mean number of unique prey taxa (± SD) Albacore tuna Bigeye tuna Dolphinfish Swordfish White marlin Yellowfin tuna Number of stomach samples Fig. 2. Cumulative prey curves for stomach samples collected for albacore tuna (Thunnus alalunga), bigeye tuna (Thunnus obesus), dolphinfish (Coryphaena hippurus), yellowfin tuna (Thunnus albacares), white marlin (Tetrapturus albidus), and swordfish (Xiphias gladius). Values represent mean7sd number of unique prey found for each stomach sample size. species based on all soft tissue contents as mean proportion by weight (MW i ) and frequency of occurrence (O i )(Chipps and Garvey, 2007). We compared weight percentages of the four main prey categories (teleosts, cephalopods, crustaceans, and other) using a Kruskal Wallis test, and a post-hoc Nemenyi Damico Wolfe Dunn test when significant differences (Po0.05) were detected. For swordfish and yellowfin tuna, we performed quantile regressions with standard errors estimated using the xy-pair bootstrap to assess relationships between prey and predator length. We performed regressions on the 25th and 75th quantiles to test for relationships between predator length and minimum and maximum prey lengths, respectively, with the quantreg package in R. Relationships between mean predator and prey lengths were explored using ordinary least squares linear regression. The remaining datasets contained a limited range of predator lengths or sample size that prevented further size comparisons. We used all prey length data pooled and separately examined all data for ommastrephid prey. For length data, we used measurements of whole prey as well as estimates based on beak and otolith lengths. All statistical analyses were performed using the program R (R Development Core Team, 2008). All values are reported as mean71 SD unless otherwise noted. 3. Results The slope of the final four data points for all prey curves differed significantly from zero, indicating that none of the cumulative prey curves for individual species reached an asymptote (Fig. 2). Sample size was insufficient to adequately reflect prey diversity for all predator species. Mantle length estimates based on beak regressions generally matched direct measurements, with a slight positive bias for larger cephalopods (Fig. 3). Validation was not performed for the smallest sampled beaks, so accuracy could not be assessed for the complete beak dataset. For prey composition, fishes and/or cephalopods occurred in higher proportions than crustaceans for all predator species

5 J.M. Logan et al. / Deep-Sea Research II 95 (2013) Estimated Length (mm) Architeuthidae Histioteuthidae Ommastrephidae Measured Length (mm) Fig. 3. Paired comparisons of cephalopod mantle lengths (mm) estimated from beak lower rostral lengths with direct measurements of whole mantle samples. A 1:1 line is included for comparison. except shortfin mako and longbill spearfish, which had no differences among prey groups (Table 2). Fishes and cephalopods were statistically indistinguishable for albacore tuna, bigeye tuna, white marlin, and swordfish. Fishes were the sole dominant prey group for blue marlin, dolphinfish, and yellowfin tuna (Table 2). Ommastrephidae made up the highest proportion of cephalopod biomass based on soft tissues and reconstituted weight from beak data for all species (Table 3). Histioteuthidae and octopoda also occurred in a high proportion for most predator species (Table 3). Architeuthidae soft tissues and beaks were present in bigeye tuna, white marlin and swordfish while beak material was found in yellowfin tuna samples. Swordfish stomachs contained the highest diversity of cephalopod prey based on both soft tissues and beaks (Table 3). While cephalopods were found in diet samples throughout the longline transect, higher proportions were generally found in the more southerly region sampled in 2002 (Fig. 4). Soft tissue stomach contents were highly variable among individual samples, cruise years, and species, but some general foraging patterns emerged (Table 3; Appendix A). Ommastrephidae was the dominant prey family overall among predator species, although large proportions of soft tissue contents contained unidentifiable fishes and cephalopods. Octopods were a consistent secondary prey group among predator species. Albacore tuna had higher proportions of crustacean prey (6.5% MW i ) than other predators, with Gadidae and Paralepididae as additional secondary prey groups. Bigeye tuna secondary prey included Exocoetidae, Ariommatidae, Stromateidae, and Myctophidae. Yellowfin tuna and dolphinfish consumed Sargassumassociated, epipelagic prey including Molidae, Exocoetidae, Monacanthidae, and Diodontidae, but yellowfin tuna stomachs also contained small proportions of meso-and bathypelagic prey (e.g., Gempylidae, Alepisauridae). Yellowfin tuna and swordfish both consumed Gempylidae as well as Bramidae. Swordfish stomachs contained a variety of secondary prey families including both fishes (e.g., Sebastidae and Diretmidae) as well as cephalopods (e.g., Architeuthidae, Loliginidae; Table 3; Appendix A). We observed significant relationships between predator and prey lengths for yellowfin tuna and swordfish (Fig. 5; Table 4). Mean and maximum (75th quantile) prey length for grouped prey increased significantly with length for both predator species. For swordfish, mean and minimum (25th quantile) prey length also increased significantly with predator length for ommastrephid prey (Fig. 5; Table 4). 4. Discussion 4.1. Cephalopod prey importance Along these broad ocean transects, the highest overall prey biomass was composed of Ommastrephidae, a widely distributed family of fast-swimming squids. Ommastrephid squids were found in all sampled predator species except blue marlin, based on soft tissue remains and cephalopod beak material. Top fish predators such as swordfish and tunas target ommastrephids and other cephalopods throughout world oceans, as confirmed previously by diet studies of swordfish in the western (Lansdell and Young, 2007) and eastern Pacific Ocean (Ibáñez et al., 2004; Markaida and Hochberg, 2005), Indian Ocean (Potier et al., 2007), Atlantic Ocean (dos Santos and Haimovici, 2000; Hernández-Garcia, 1995; Moreira, 1990; Santos et al., 2001; Toll and Hess, 1981), and Mediterranean Sea (Bello, 1991; Peristeraki et al., 2005; Salman, 2004). Ommastrephid squids were also important prey for swordfish along the northern (Scott and Tibbo, 1968) and southern (Toll and Hess, 1981) sections of our sampling region. Similarly, in the eastern and tropical central Atlantic, ommastrephid squids were prevalent in diets of all of the billfish and tuna species sampled in our study (Cherel et al., 2007; Pelczarski, 1988; Sim~oes and Andrade, 2000). While we did not sample a wide variety of sharks (only two shortfin makos were analyzed), ommastrephids were the dominant identifiable prey family (10.6% MW i ), consistent with past studies in the North Atlantic (Stillwell and Kohler, 1982). Our results are similar to historical findings demonstrating major contributions of Ommastrephidae to the diets of large pelagic fishes in the central North Atlantic Ocean (Matthews et al., 1977), suggesting that they have remained available to Table 2 Mean weight percentages (MW i )7SD of the four prey categories (cephalopods, fishes, crustaceans, and other). The other category consists of unidentifiable material, parasites, algae, bivalves, gastropods, and heteropods. Weight percentages in a given row with different letter superscripts are significantly different (Po0.05 following Holm adjustment) based on Nemenyi Damico Wolfe Dunn post-hoc comparisons. Fishes Cephalopods Crustaceans Other MW i (%) O i (%) MW i (%) O i (%) MW i (%) O i (%) MW i (%) O i (%) Albacore tuna a a b b 32.1 Bigeye tuna a a,b c b,c 28.6 Blue marlin a,c b b b,c 66.7 Dolphinfish a b b b 90.9 Shortfin mako a a a a 50.0 White marlin a a,b b b 44.4 Longbill spearfish a a a a 66.7 Yellowfin tuna a b c b,c 50.0 Swordfish a a b b 63.8

6 78 J.M. Logan et al. / Deep-Sea Research II 95 (2013) Table 3 Cephalopod stomach contents based on beak and soft tissues. Data are presented as mean percent weight (MW i )7SD followed by mean percent occurrence (O i )in parentheses. Beak and soft tissue data are reported in bold and italics, respectively. Cephalopod remains were not found in any blue marlin samples. Prey Albacore tuna Bigeye tuna Dolphinfish Longbill spearfish White marlin Yellowfin tuna Shortfin mako Swordfish Teuthoidea (88.9) (94.1) (88.9) Unidentifiable (70.6) (66.7) (80.0) (83.3) (50.0) (83.3) (85.7) (71.4) (86.7) (94.7) (84.2) (95.2) (98.0) (85.7) Architeuthidae (6.7) (11.9) (11.1) (16.7) (4.1) (11.1) (14.3) Chiroteuthidae (12.5) (20.0) (13.3) (7.1) Cranchiidae (2.4) Cycloteuthidae (20.0) Enoploteuthidae (11.1) (4.8) (2.0) Gonatidae (19.1) (4.1) Histioteuthidae (23.8) (50.0) (22.2) (40.0) (33.3) (33.3) (11.8) (11.1) (10.5) (2.0) Loliginidae (2.0) Ommastrephidae (87.5) (66.7) (60.0) (66.7) (73.3) (78.6) (41.2) (66.7) (50.0) (28.6) (44.4) (33.3) (28.6) (26.3) Onychoteuthidae (7.1) Vampyroteuthidae (2.4) Octopoda (25.0) (14.3) (33.3) (80.0) (33.3) (60.0) (5.9) (11.1) (16.7) (14.3) (21.1) (4.1) predators in these open ocean food webs since the onset of industrialized fishing. A recent trophic study of large pelagic fishes in the Gulf Stream also showed consistency in diet over the past several decades (Rudershausen et al., 2010). The apparent dietary stability in the Gulf Stream and central North Atlantic could be partly due to the ecological redundancy of these pelagic ecosystems in which a diverse array of pelagic fishes feed on similar prey (Griffiths et al., 2010). Ommastrephid distribution and abundance fluctuate with oceanographic conditions (Dawe and Warren, 1993; Dawe et al., 2000, 2007), and changes in this prey resource may have occurred in the past between sampling periods due to bottom up rather than top down processes. Future ocean warming could influence the availability of this cephalopod prey resource for large pelagic fishes through changes in timing and location of annual peak abundance (Sims et al., 2001). Further studies linking cephalopod distribution and abundance to oceanographic variables are needed to better predict potential ecosystem effects associated with climate change. Cephalopods were only identified to the family level, but previous diet studies and cephalopod surveys in the region of our study provide evidence of potential dominant prey species. For the more northerly sampling regions, the ommastrephid prey were likely made up mostly of shortfin squid, Illex illecebrosus,andotherillex species. In submersible surveys and pelagic trawls along the continental slope of the U.S. East Coast, Illex spp. were the most commonly observed cephalopods (Gartner et al., 2008; Vecchione and Pohle, 2002). Shortfin squid were the main cephalopod prey identified for swordfish along the continental slope for the latitudes sampled in 2001 and the northern latitudes samples in 2002 (Cape Hatteras, North Carolina to the Grand Banks) (Stillwell and Kohler, 1985). Shortfin squid were also important prey for swordfish sampled on the Grand Banks (Scott and Tibbo, 1968). Illex spp. were documented as important prey for swordfish in the Straits of Florida, near the southern range of our survey (Toll and Hess, 1981). In the historical survey by Matthews et al. (1977), Illex spp. were important cephalopod prey for a variety of tuna species. In addition to Illex spp., Matthews et al. (1977) also observed Ommastrephes spp. and Ornithoteuthis antillarum. For the southern portion of our survey, ommastrephid squid prey could have included O. antillarum and the orangeback flying squid, Sthenoteuthis pteropus, which were both identified in the diets of large pelagic fishes slightly south of our sampling region (Cherel et al., 2007). O. antillarum was also commonly observed in this southern region in a previous submersibles survey (Vecchione and Roper, 1991). Secondary cephalopod prey from our study included Histioteuthidae, Gonatidae, octopoda, and Architeuthidae. Based upon historical diet studies (Matthews et al., 1977; Toll and Hess, 1981) and cephalopod surveys (Vecchione and Pohle, 2002), histioteuthid prey were likely of the genus Histioteuthis. The gonatid prey were likely of the genus Gonatus. G. steenstrupi was the most abundant cephalopod sampled in trawl surveys north of our sampling region (Vecchione et al., 2010) while G. fabricii was abundant in previous tuna diet studies (Matthews et al., 1977). For octopod prey, Argonauta has been identified in diets of swordfish and tunas throughout our sampling region (Matthews et al., 1977; Toll and Hess, 1981) and species of this genus were likely present in our samples. Other octopods identified in previous diet studies include Japetella diaphana and Allopsus mollis (Matthews et al., 1977; Toll and Hess, 1981). Architeuthidae, likely Architeuthis dux (Aldrich, 1991), was observed in swordfish, bigeye tuna, yellowfin tuna, and white marlin stomachs. While Architeuthidae has been observed previously in swordfish diet studies, to our knowledge these are the first observations for the latter pelagic predator species.

7 J.M. Logan et al. / Deep-Sea Research II 95 (2013) These results agree with past diet studies for yellowfin tuna in the Pacific Ocean (Graham et al., 2007; Ménard et al., 2006; Young et al., 2010) that showed an ontogenetic increase in prey length and trophic position. For both swordfish and yellowfin tuna, we observed significant increases in mean prey size, but no increase in minimum prey size for all prey. This pattern is consistent with consumption of larger prey by larger yellowfin tuna and swordfish, but continued consumption of small prey. For swordfish in the Pacific Ocean, both minimum and maximum prey size increased with predator length (Young et al., 2010). Ontogenetic shifts from crustacean to ommastrephids and other larger prey were observed for swordfish in the central eastern Atlantic (Velasco and Quintans, 2000). Nitrogen stable isotopes (d 15 N), a proxy for trophic position (Post, 2002), from swordfish sampled during the central North Atlantic survey showed an increasing trend with swordfish length (Logan and Lutcavage, 2013), further supporting an ontogenetic dietary shift to higher trophic level prey Data limitations and conclusions Fig. 4. Quantiles of (A) mean percent weight (MW i ) data for cephalopod soft tissue and mean number of cephalopod families (MN i ) for (B) soft tissue and (C) beak material pooled across all stomach samples for each longline set location. In panels (B) and (C), unidentifiable Teuthoidea samples were counted as an additional family category Prey size relationships Stomach content data indicated increasing trends in prey size in relation to predator size for yellowfin tuna and swordfish. The exploratory longline cruises producing our results were conducted in 2001 and 2002 to establish the biological status of Atlantic bluefin tuna (Thunnus thynnus) and other large pelagic species in the central North Atlantic (Lutcavage and Luckhurst, 2001), with additional legs conducted in more equatorial areas (Satoh et al., 2004). While these and other historic research cruises intercepted top fish predators in the important transition region between the Gulf Stream boundary current, the north Sargasso Sea, and continental shelf, large gaps in sampling remain. Even with over 50 years of commercial exploitation of top predators in the Atlantic, there is only cursory scientific understanding of the dietary roles of pelagic squids and fishes. Without such ecological information, it is difficult to assess the status of top fish predators or the food webs needed to rebuild populations that remain overexploited. In a review of sources of variation and error in the study of top predator diets, Santos et al. (2001) caution against ignoring sources of bias related to food habit studies of fishes, seabirds, and marine mammals. Sampling of tunas and billfishes conducted via fishing operations can be biased by bait and chum (Chase, 2002), and both squid (Illex sp.) and Atlantic mackerel (Scomber scombrus) were used as bait during the sampling cruises. The presence of a wide range of ommastrephid sizes at varying stages of digestion suggests that a high proportion of those found in stomach contents were natural prey, although outlier isotope data suggest that the ommastrephid prey group may have contained some bait (Logan and Lutcavage, 2013). Inadequate sample sizes were the main limiting factor for this study, as cumulative prey curves indicated that sample sizes were insufficient to characterize prey diversity. Future diet studies in the central North Atlantic would benefit from increased sample sizes, species-level prey identification, and complementary tracers (e.g., stable isotopes, fatty acids) to provide a more comprehensive evaluation of trophic structure in this region. Despite limited sample sizes, our study provides additional evidence of the importance of ommastrephid squids and other cephalopods as prey for large pelagic fishes in open ocean food webs in the central North Atlantic and worldwide. 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

8 80 J.M. Logan et al. / Deep-Sea Research II 95 (2013) Prey length (cm) Predator length (cm) Prey length (cm) Predator length (cm) Prey length (cm) Predator length (cm) Prey length (cm) Predator length (cm) Fig. 5. Predator prey size relationships for yellowfin tuna (Thunnus albacares) (A, B) and swordfish (Xiphias gladius) (C, D) for all measured (A, C) prey and all measured ommastrephid prey (B, D). Solid lines represent upper (75th) and lower (25th) quantile regression lines. Dashed lines represent least squares regression lines. Table 4 Quantile and linear regression results comparing lengths of prey relative to swordfish (Xiphias gladius) and yellowfin tuna (Thunnus albacares) lengths. Prey lengths consist of measurements from whole prey items and estimates based on relationships between otolith and beak lengths with fork and mantle length, respectively. Comparisons were made for all prey items and separately for all ommastrephid squid prey items. All Prey Swordfish (n¼48) cm FL Yellowfin tuna (n¼17) cm FL Equation p-value Equation p-value Mean Y¼0.1787x (SE S ¼0.0465; SE i ¼8.0749) n Y¼0.0517xþ (SE S ¼0.0186; SE i ¼2.3868) n 25th percentile Y¼0.0932x (SE S ¼0.0554; SE i ¼8.5456) Y¼0.0241xþ (SE S ¼0.0242; SE i ¼3.0616) th percentile Y¼0.1806xþ (SE S ¼0.0677; SE i ¼ ) n Y¼0.0491xþ (SE S ¼0.0183; SE i ¼2.2997) n Ommastrephid Prey Swordfish (n¼29) cm FL Yellowfin tuna (n¼11) cm FL Mean Y¼0.1207xþ (SE S ¼0.0577; SE i ¼ ) n Y¼0.0203xþ (SE S ¼0.0159; SE i ¼2.0544) th percentile Y¼0.1569x (SE S ¼0.0677; SE i ¼ ) n Y¼0.0266xþ (SE S ¼0.0159; SE i ¼1.9237) th percentile Y¼0.0827xþ (SE S ¼0.0577; SE i ¼9.8538) Y¼0.0366xþ (SE S ¼0.0249; SE i ¼3.6877) Standard error estimates based on bootstapping are listed for slope (SE s ) and intercept (SE i ). n Significant p-values (po0.05). (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, Larry Harris, Karsten Hartel, Cheryl Harary, Piper Bartlett, Jillian Armstrong Pamela Polloni, and the late James E. Craddock for help with prey evaluations. We would also like to thank Michelle Staudinger, Frédéric Ménard, and an anonymous reviewer for their helpful comments on earlier drafts of this manuscript. 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. Appendix A. Supplementary material Supplementary data associated with this article can be found in the online version at References Aldrich, F.A., Some aspects of the systematics and biology of squid of the genus Architeuthis based on a study of specimens from Newfoundland waters. Bull. Mar. Sci. 49 (1 2),

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