Feeding Habits Variability and Trophic Position of Dolphinfish in Waters South of the Baja California Peninsula, Mexico

Transcription

1 This article was downloaded by: [Department Of Fisheries] On: 12 August 2014, At: 20:55 Publisher: Taylor & Francis Informa Ltd Registered in England and Wales Registered Number: Registered office: Mortimer House, Mortimer Street, London W1T 3JH, UK Transactions of the American Fisheries Society Publication details, including instructions for authors and subscription information: Feeding Habits Variability and Trophic Position of Dolphinfish in Waters South of the Baja California Peninsula, Mexico Y. E. Torres-Rojas ab, A. Hernández-Herrera a, S. Ortega-García a & M. F. Soto-Jiménez b a Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Avenida Instituto Politécnico Nacional, s/n Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur 23096, Mexico b Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de Mexico, Avenida Joel Montes Camarena, s/n Colonia Playa Sur, Mazatlán, Sinaloa, Mexico Published online: 13 Mar To cite this article: Y. E. Torres-Rojas, A. Hernández-Herrera, S. Ortega-García & M. F. Soto-Jiménez (2014) Feeding Habits Variability and Trophic Position of Dolphinfish in Waters South of the Baja California Peninsula, Mexico, Transactions of the American Fisheries Society, 143:2, , DOI: / To link to this article: PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the Content ) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at

2 Transactions of the American Fisheries Society 143: , 2014 C American Fisheries Society 2014 ISSN: print / online DOI: / ARTICLE Feeding Habits Variability and Trophic Position of Dolphinfish in Waters South of the Baja California Peninsula, Mexico Y. E. Torres-Rojas* Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Avenida Instituto Politécnico Nacional, s/n Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur 23096, Mexico; and Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de Mexico, Avenida Joel Montes Camarena, s/n Colonia Playa Sur, Mazatlán, Sinaloa, Mexico A. Hernández-Herrera and S. Ortega-García Instituto Politécnico Nacional, Centro Interdisciplinario de Ciencias Marinas, Avenida Instituto Politécnico Nacional, s/n Colonia Playa Palo de Santa Rita, La Paz, Baja California Sur 23096, Mexico M. F. Soto-Jiménez Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de Mexico, Avenida Joel Montes Camarena, s/n Colonia Playa Sur, Mazatlán, Sinaloa, Mexico Abstract Using data from analyses of stomach contents and stable isotopes, we examined high-resolution variations in the feeding habits and trophic position of Dolphinfish Coryphaena hippurus during In total, 418 specimens were collected off the southern Baja California peninsula, Mexico. Based on analysis of stomach contents (% index of relative importance [%IRI]), Dolphinfish consumed mainly epipelagic prey, with the red crab Pleuroncodes planipes as the most abundant prey species. The diet was highly similar between sexes but differed between size-classes: Dolphinfish smaller than 65 cm FL fed mainly on Pacific Sardine Sardinops sagax caeruleus (%IRI = 30), whereas those larger than 110 cm FL fed mainly on jumbo squid Dosidicus gigas (%IRI = 45) in addition to red crabs. Dietary differences between the smallest and largest specimens were mainly related to changes in morphology and spatial stratification by size (i.e., to avoid cannibalism). Trophic positions estimated by both methods indicated that the Dolphinfish is a secondary to tertiary carnivore with a high degree of trophic plasticity, and thus it plays different trophic roles within the area. Elevated variability in δ 15 N and Shannon Wiener diversity index values on an annual scale revealed that Dolphinfish are opportunistic predators. Interannual diet variation related to the availability and abundance of prey species can be explained by changes in environmental conditions due to climate anomalies associated with El Niño Southern Oscillation events. We highlight that the Dolphinfish is a good indicator of changes occurring in the food web structure of pelagic ecosystems. The observed variations in feeding habits and trophic position are critical to understanding the ecology and role of Dolphinfish in marine ecosystems by providing knowledge on feeding locations, seasonal prey utilization, and prey availability and allowing predictions of possible ecological responses to environmental change. 528 *Corresponding author: yassirtorres@gmail.com Received January 11, 2013; accepted November 12, 2013

3 FEEDING HABITS AND TROPHIC POSITION OF DOLPHINFISH 529 The Dolphinfish Coryphaena hippurus is an epipelagic species with a worldwide distribution. Throughout much of its range, the Dolphinfish is in high demand for human consumption (Herzig 1990); as a result, it is targeted by and caught as bycatch in commercial, artisanal, and recreational fisheries in many coastal countries (Wu et al. 2001; Schwenke et al. 2008), including Mexico (Zúñiga-Flores et al. 2008; Tripp-Valdez et al. 2010). The coastal area along the southern Baja California peninsula near Cabo San Lucas, Baja California Sur, is the most productive sport fisheries area in Mexico, with an annual income of US$54 million (Ditton et al. 1996). Although they are most abundant during the summer, Dolphinfish are available year-round in the waters around the Cabo San Lucas area. The life span of Dolphinfish averages 2 years, with sexual dimorphism noticeable after 6 months of age (Benetti et al. 1995); males are physically larger and heavier than females of the same age (Ditty et al. 1994). Dolphinfish are an important component of the pelagic food web in the eastern Pacific Ocean, exhibiting spatial segregation by size (Olson and Galván-Magaña 2002). Stomach content analyses indicate that off the southern Baja California peninsula, Dolphinfish are opportunistic predators that consume a broad range of prey items (e.g., red crab Pleuroncodes planipes) mainly in the epipelagic zone, but no shift in function between sizes or sexes has been observed (Aguilar- Palomino 1993). Although stomach content analyses provide detailed information about the diets consumed by fish, this method does not account for long-term patterns of nutrient transfer (e.g., months) and instead provides only an instantaneous measure of an organism s diet (Vander Zanden et al. 1997). This problem underscores the potential biases in the conclusions made by Aguilar- Palomino (1993), who reported that Dolphinfish off the southern Baja California peninsula did not undergo ontogenetic shifts in diet. Stable isotope analysis has emerged as a valuable complement to traditional stomach content analyses in dietary studies because it provides a time-integrated dietary representation and characterization of trophic relationships over a scale of months (Buchheister and Latour 2010). The combination of stomach content analysis and stable isotope analysis has been useful for detecting variations in the feeding habits and trophic position of shrimps and demersal fishes in marine ecosystems (Fanelli and Cartes 2008, 2010). Knowledge of feeding habits and trophic position through time for keystone species such as the Dolphinfish will provide information about the species predatory role and how these species interact with other species in the community (Olson and Galván-Magaña 2002). Such information could be very useful for the management of Dolphinfish and other predator and prey populations along the southern Baja California peninsula (Essington et al. 2002) and could provide a better comprehension of the structure and function of marine communities and ecosystems in this area and elsewhere. Climate variability and climate change impacts on marine species have become a new focus of research in pelagic ecosystems (Hobday et al. 2013). Large pelagic species like the Dolphinfish can be used as indicators of an ecosystem s status and of climate change impacts because such species are dependent upon an extensive set of trophic links within the wider marine food web (Thompson and Ollason 2001; Hobday and Evans 2013). It is important to consider feeding ecology and climate variability when assessing variability in exploited species and when designing management responses to climate or fisheries threats. We used a combination of stomach content analysis and stable isotope analysis to (1) corroborate that the prey species exploited by Dolphinfish in the study area do not vary with Dolphinfish sex or size, (2) examine interannual changes in Dolphinfish feeding habits and trophic position in order to better understand this species role in the region, and (3) evaluate changes in feeding habits due to natural climate variability (e.g., El Niño Southern Oscillation [ENSO]), which could reflect ecosystem changes associated with climatic fluctuations. This information is important for ecosystem modeling efforts, which require quantitative data on food web relationships over longer time periods that are more relevant to ecosystem processes, and could be very useful for developing future scenarios and adaptation options. METHODS Samples were obtained from recreational fishery landings in the area of Cabo San Lucas, Baja California Sur, Mexico ( N, W). The recreational fishing fleet operates within a range of km (30 nautical mi) from the coastline (Abitia-Cárdenas et al. 1997). This fishing area is influenced by the presence of different water masses, including water from the California Current, equatorial surface water, water from the Gulf of California, subtropical subsurface water, and Costa Rica water (Álvarez et al. 1978; Molina-Cruz 1986; Lavín et al. 1997), in addition to oceanic fronts that result in high productivity (Álvarez-Borrego 1983). Sample collection and processing. Samples of Dolphinfish were collected monthly during the summer (May November) over a period of 3 years ( ). The FL (cm) and sex of each specimen were recorded. In the laboratory, frozen stomachs were thawed, and prey items were identified to the lowest possible taxonomic level and separated for further analyses. Stomach contents were immediately analyzed to obtain information on recently consumed food, and muscle tissue samples were collected for stable isotope analysis to obtain information on the time-integrated diet. Ten potential prey types consumed by Dolphinfish (based on Aguilar-Palomino et al. 1998) were simultaneously collected during this study by using a gill net (mesh size = cm [2.25 in]). Prey specimens were identified, biometric measurements were taken, and the specimens were then dissected to obtain muscle tissue. Tissue samples were kept frozen ( 20 C) until further analysis at the fish laboratory of the Centro Interdisciplinario de Ciencias Marinas in La Paz, Baja California Sur.

4 530 TORRES-ROJAS ET AL. The following keys were used to identify fishes: Clothier (1950), Monod (1968), Miller and Lea (1972), Miller and Jorgensen (1973), Allen and Robertson (1994), Fischer et al. (1995), and Thomson et al. (2000). Cephalopods were identified based on their beaks according to Iverson and Pinkas (1971), Wolff (1982, 1984), and Clarke (1986). Crustaceans were identified based on Fischer et al. (1995). For isotopic analyses, Dolphinfish and prey samples were placed in vials fitted with Teflon lids and were then dried for 24 h in a Labconco lyophilizer at a temperature of 45 C and pressure of to millibars. The samples were then ground in an agate mortar. Lipids were not removed from these samples prior to analysis. Subsamples (1 mg) were weighed using an Ohaus analytic scale ( ± g precision) and were stored in tin capsules (8 5 mm). The carbon isotope (δ 13 C) and nitrogen isotope (δ 15 N) compositions were determined at the Stable Isotope Laboratory (Department of Agronomy, University of California, Davis) by using an isotope ratio mass spectrometer (20-20 mass spectrometer; PDZ Europa Scientific, Sandbach, UK) with a precision of The C:N ratio was calculated from values obtained with an elemental analyzer coupled to the isotope ratio mass spectrometer. Data analysis. To detect intraspecific diet variation, we sorted the data by Dolphinfish sex, Dolphinfish size-class (46 65, , , , and cm FL; Olson and Galván-Magaña 2002), and collection year. We constructed cumulative prey curves for each category to determine whether the number of stomachs analyzed was representative of the trophic spectrum of Dolphinfish (Ferry and Cailliet 1996). The observed data matrix of the number of stomachs (i.e., unit effort) versus the accumulated prey items was randomized 100 times to obtain an ideal curve of species accumulation (EstimateS program; Colwell 2006). As an indicator of the degree of variability in the diet, the CV was calculated for all stomachs (for this study, a CV less than 0.05 was considered adequate) to represent the trophic spectrum of Dolphinfish (Steel and Torrie 1992). Finally, the diversity of prey types was plotted in relation to the number of stomachs analyzed. Estimates of feeding habits. The index of relative importance (IRI) was calculated as follows: IRI = (%N + %W) (%F), where %N is the number of individuals of each prey type and %W is the wet weight of each prey type, expressed as a percentage of the total number or weight of all prey items in the stomach contents. The frequency of occurrence of each food item (i.e., presence or absence) in all stomachs that contained food was originally described by Pinkas et al. (1971) and subsequently modified as a percentage (%F) bycortés (1997). To determine whether there were differences in diet between sexes, among size-classes, or among years, similarity was analyzed using permutation randomization methods in a Bray Curtis dissimilarity matrix (analysis of similarity [ANOSIM] in PRIMER 6 version 6.1.6). The global rank dissimilarity value, R ANOSIM (0 R ANOSIM 1), is a useful comparative measure of the degree of separation. When R ANOSIM is near zero, the null hypothesis cannot be rejected that is, there is no separation between groups (Clarke and Warwick 2001). The Shannon Wiener diversity index (H ) based on the abundance of all prey types was used to calculate diversity (Pielou 1975): s H = (p i )log e (p i ), i=1 where p i is the numerical fraction of individuals belonging to the ith prey species. The breadth of the Dolphinfish s trophic niche was evaluated by using Levin s standardized index, Bi (Krebs 1999). The Bi ranges in value from 0 to 1, with low values (<0.6) indicating a diet dominated by few prey types (i.e., a specialist predator) and higher values (>0.6) indicating a generalist predator (Labropoulou and Eleftheriou 1997): 1 Bi = n 1 [( 1/ ) )], Pji 2 1 where Bi is Levin s index for predator j; Pji 2 is the numerical proportion of the ith prey type in predator j s diet; and n is the number of prey categories. The δ 13 C and δ 15 N values were compared graphically between sexes, among size-classes, and among years. A Mann Whitney U-test was used to compare between males and females, and an ANOVA test by ranks (Kruskal Wallis ANOVA) was used to identify significant differences among size-classes and among years. If differences were detected, Dunn s post hoc test was used to identify the source of variation. Spearman s rank correlation analysis of prey size (e.g., fish, crustaceans, and cephalopods) versus Dolphinfish size was used to test whether prey size had significant effects on the Dolphinfish s diet (Zar 1999). Estimates of trophic position. The trophic positions of Dolphinfish and their prey were calculated based on the results of both stomach content analysis and stable isotope analysis. The trophic position based on stomach content analysis was calculated using the equation proposed by Christensen and Pauly (1992): ( n ) TP stomach = 1 + DC ji (TP i ), where DC ji is the diet composition by weight in terms of the proportion of prey type i in the diet of predator j; TP i is the trophic position of prey type i; and n is the number of prey types in the diet. Trophic position values for prey fish species were obtained from FishBase (Froese and Pauly 2003), and those for cephalopods and crustaceans were obtained from Cortés (1999). The trophic position based on stable isotope analysis was calculated with the following equation (Post 2002): i=1 TP isotope = λ + (δ15 N Predator δ 15 N Base ) n,

5 FEEDING HABITS AND TROPHIC POSITION OF DOLPHINFISH 531 where δ 15 N Predator is the N isotopic composition of each Dolphinfish; λ is the trophic position of the organism used to estimate δ 15 N Base. The N isotopic composition of the food base (δ 15 N Base ) in the area of the southern Baja California peninsula during summer was composed mainly of phytoplankton (diatoms: average δ 15 N = 5.7 ; λ = 1; White et al. 2007). The n represents the theoretical trophic enrichment assumed to be 3.4 for all trophic estimations (Post 2002). We estimated the contribution of each prey type to the diet by using the Bayesian mixing model MixSIR version (Moore and Semmens 2008), which takes into account isotopic errors by using as inputs all δ 13 C and δ 15 N values of predators and the mean (± SD) δ 13 C and δ 15 N values of the prey types. The results of this analysis are reported as the distribution of percentages ranging from 0% to 99%, where the minimum and maximum values are used to determine the importance of food sources or prey types to the diet (Madigan et al. 2012). RESULTS In total, 418 individual Dolphinfish were caught during May November over a 3-year period ( ). The ratio of males to females was 1.10, and the ratio of small (<65 cm FL) to large (>110 cm FL) individuals was 1.55 (Table 1). Of the 418 stomachs that were examined, 359 (86%) contained food and H bits/ind TABLE 1. Summary description of Dolphinfish samples used for stomach content analysis (SCA) and stable isotope analysis (SIA) by sex, size-class (based on Olson and Galván-Magaña et al. 2002), and sampling year. Year Category Group Technique Sex Male SCA SIA Female SCA SIA Size-class (cm FL) SCA SIA SCA SIA SCA SIA SCA SIA SCA SIA (14%) were empty. The prey species accumulation curve showed that the number of stomachs we analyzed was sufficient for characterizing the Dolphinfish s diet (Figure 1), with CVs less than 0.05 for all categories (i.e., sexes, size-classes, and C.V stomachs = C.V Number of Stomachs FIGURE 1. General cumulative curve of prey species consumed by Dolphinfish (black line = Shannon Wiener diversity index [H ] ± SD, bits/ind [bits/individual]; gray line = CV).

6 532 TORRES-ROJAS ET AL. TABLE 2. Coefficients of variation (CVs) for the prey species accumulation curves and the C:N ratio of Dolphinfish by sex, size-class (based on Olson and Galván-Magaña 2002), and sampling year. Cumulative number of stomach samples to reach a CV 0.05 Category Group (CV in parentheses) C:N (SD) Sex Male 129 (0.041) 3.18 (0.09) Female 141 (0.046) 3.26 (0.24) Size-class (cm FL) (0.043) 3.18 (0.07) (0.049) 3.23 (0.14) (0.045) 3.20 (0.12) (0.047) 3.18 (0.07) (0.050) 3.23 (0.09) Year (0.040) 3.20 (0.12) (0.050) 3.20 (0.09) (0.050) 3.30 (0.20) years; Table 2). The C:N ratios for muscle were between 3.0 and 3.5 and averaged 3.2 (Table 2), which corresponds to low lipid concentrations in the tissue (Post et al. 2007). Thus, the effect of lipid content on the δ 13 C values in this study was considered negligible, and the chemical extraction of lipids before isotopic analysis or an arithmetic correction based on the C:N ratio was not required. The average δ 15 N value ( ± SD) for dorsal muscle was ± 1.82 (range = ), and the average δ 13 C value was ± 0.53 (range = to ). The trophic position of Dolphinfish varied from 3.6 to 4.0 based on stomach content analysis and from 3.2 to 4.0 based on stable isotope values (Table 3). The trophic positions estimated with these two methods were not significantly different (Kruskal Wallis ANOVA: H 1, 355 = 1.53, P = 0.21). Dolphinfish Prey Types The trophic spectrum of Dolphinfish was composed of 13 cephalopod species representing 8 families; 11 crustacean species representing 8 families; 63 fish species representing 26 families; and 1 sea turtle species (Table 4). Prey types varied in size from 2 to 18 cm for cephalopods, from 2.0 to 19.5 cm for crustaceans, and from 3 to 55 cm for fishes. According to the percent IRI (%IRI), the main prey species of Dolphinfish were the red crab (58.1%), jumbo squid Dosidicus gigas (6.0%), mackerels Auxis spp. (4.2%), and Bigeye Scad Selar crumenophthalmus (4.1%). In total, 35 muscle samples from the 10 most common prey types (which together accounted for over 80% of the IRI in the study area; Table 4) were analyzed for δ 15 N and δ 13 C values (Table 5). The δ 15 N values (mean ± SD) ranged from 7.95 ± 1.69 (red crab) to ± 1.18 (Deepwater Cornetfish Fistularia corneta), while the δ 13 C values ranged from ± 1.55 (red crab) to ± 0.36 (Oceanic Puffer Lagocephalus lagocephalus). Based on the mixing model results, the main prey types consumed by Dolphinfish were the red crab (48 56%), Auxis spp. (0 33%), the Pacific Sardine Sardinops sagax caeruleus (0 29%), and the Oceanic Puffer (0 28%). Comparison of Diet by Sex According to the%iri, the red crab was the most important component of the diets for Dolphinfish males and females (>55%). The ANOSIM showed no diet separation between sexes (R ANOSIM = 0.01). The diversity index (H ) value was similar between males (H = 2.37) and females (H = 2.33), and the diet breadth (Bi) values were less than 0.6 for both sexes (Bi males = 0.02; Bi females = 0.03). No significant differences in isotopic values were observed between the sexes (Mann Whitney U-test, δ 15 N: U = 197.0, P = 0.06; δ 13 C: U = 284.0, P = 0.96; Figure 2). Trophic position estimated based on stomach content analysis (U = 11,609.5, P = 0.32) or based on δ 15 N TABLE 3. Isotopic composition (δ 13 Candδ 15 N, ) and trophic position (based on stomach content analysis [TP stomach ]orδ 15 N composition [TP isotope ]) of Dolphinfish collected off the southern Baja California peninsula (SD is given in parentheses). Data are summarized by sex, size-class (based on Olson and Galván-Magaña 2002), and sampling year. Category Group Average δ 15 N Average δ 13 C TP stomach TP isotope Sex Male (1.89) (0.57) 3.9 (0.5) 3.5 (0.5) Female (1.66) (0.61) 3.9 (0.6) 3.7 (0.4) Size-class (cm FL) (1.32) (0.35) 3.6 (0.6) 4.0 (0.4) (1.80) (0.41) 3.8 (0.5) 3.8 (0.5) (1.37) (0.56) 3.9 (0.5) 3.5 (0.4) (2.10) (0.63) 4.0 (0.4) 3.6 (0.6) (1.24) (0.31) 3.9 (0.5) 3.2 (0.3) Year (1.94) (0.52) 3.9 (0.5) 3.6 (0.6) (1.17) (0.49) 4.0 (0.6) 3.7 (0.3) (2.00) (0.72) 3.8 (0.6) 3.7 (0.6)

7 FEEDING HABITS AND TROPHIC POSITION OF DOLPHINFISH 533 TABLE 4. Composition of stomach contents from Dolphinfish collected off the southern Baja California peninsula during Values in bold italics represent the most important prey items in the Dolphinfish s diet based on the index of relative importance (IRI; N = number of individuals of the given prey type in the stomach contents; %N = number expressed as a percentage of all prey items; W = wet weight of the given prey type; %W = wet weight expressed as percentage of the total weight of all prey items; F = frequency of occurrence; %F = percentage frequency of occurrence; x = no data; * = number of stomachs that contained prey). Mean prey Order or family Species or group TL, cm (SD) N %N W %W F %F IRI %IRI Cephalopods Teuthoidea Theutoids x Bolitaenidae Japetella diaphana x Argonautidae Paper nautiluses Argonauta spp. 4.6 (1.8) Argonauta cornutus 2.3 (1.0) Argonauta nouryi 2.0 (1.0) Ancistrocheiridae Ancistrocheirus lesueurii x Enoploteuthidae Abraliopsis affinis x Histioteuthis dofleini x Mastigoteuthidae Mastigoteuthis dentata x Ommastrephidae Sthenoteuthis oualaniensis x Jumbo squid Dosidicus gigas 11.6 (6.0) , Other Other cephalopods x Crustaceans Nannosquillidae Nannosquillids x Portunidae Swimming crabs Callinectes spp. x Callinectes arcuatus x Callinectes bellicosus Euphylax dovii x Euphylax robustus x Portunus xantusii 3.5 (0.5) Galatheidae Red crab Pleuroncodes planipes 4.1 (1.4) , , Penaeidae Penaeid shrimps x Farfantepenaeus spp. x Farfantepenaeus brevirostris Litopenaeus vannamei x Euphausiidae Nyctiphanes simplex 4.4 (1.5) Lophogastridae Neognathophausia ingens Other Other crustaceans x Teleost Fishes Clupeidae Flatiron Herring Harengula thrissina 6.6 (1.0) Striped Herring Lile stolifera Thread herrings Opisthonema spp (1.7) Pacific Sardine Sardinops sagax caeruleus 7.5 (3.0) Engraulidae Anchovies Anchoa spp. x Phosichthyidae Panama Lightfish Vinciguerria lucetia 6.0 (1.0) Atherinidae Pitcher Silverside Atherinella nepenthe 11.0 (0.5) Belonidae Belonids (needlefishes) x Houndfish Tylosurus crocodilus fodiator x Hemiramphidae Yellowtip Halfbeak Hemiramphus marginatus x Atlantic Silverstripe Halfbeak Hyporhamphus unifasciatus x Smallwing Flyingfish Oxyporhamphus micropterus 16.2 (4.9) Exocoetidae Exocoetids (flyingfishes) Butterfly Flyingfish Cheilopogon papilio 16.0 (1.0) Beautyfin Flyingfish Cypselurus callopterus 20.0 (0.5) Tropical Two-wing Flyingfish Exocoetus volitans Sharpchin Flyingfish Fodiator acutus rostratus x Bladewing Flyingfish Hirundichthys marginatus 17.3 (6.4) , Holocentridae Panamic Soldierfish Myripristis leiognathus Fistulariidae Reef Cornetfish Fistularia commersonii Deepwater Cornetfish Fistularia corneta , Syngnathidae Pacific Seahorse Hippocampus ingens Serranidae Sand Perches Diplectrum spp Priacanthidae Glasseye Snapper Heteropriacanthus cruentatus x Echeneidae Slender Suckerfish Phtheirichthys lineatus x Carangidae Carangids (jacks) x Caranx spp. x Green Jack Caranx caballus 18.2 (10.4) , (Continued on next page)

8 534 TORRES-ROJAS ET AL. TABLE 4. Continued. Order or family Species or group Mean prey TL, cm (SD) N %N W %W F %F IRI %IRI Bigeye Trevally Caranx sexfasciatus x Pacific Bumper Chloroscombrus orqueta 24.5 (1.0) Shortfin Scad Decapterus macrosoma 24.0 (0.5) Scads Decapterus spp (1.0) Bigeye Scad Selar crumenophthalmus 19.6 (7.0) , Moonfishes Selene spp. x Pompanoes Trachinotus spp. x Nematistiidae Roosterfish Nematistius pectoralis x Coryphaenidae Dolphinfishes Coryphaena spp. x Pompano Dolphinfish Coryphaena equiselis Dolphinfish Coryphaena hippurus 44.5 (0.5) Lutjanidae Pacific Red Snapper Lutjanus peru Haemulidae Spottail Grunt Haemulon maculicauda Sciaenidae Sciaenids (drums and croakers) x Shortfin Corvina Cynoscion parvipinnis x Pacific Drum Larimus pacificus x Chaetodontidae Barberfish Johnrandallia nigrirostris x Mugilidae Mullets Mugil spp. x Striped Mullet Mugil cephalus Hospe Mullet Mugil hospes 7.5 (0.5) Sphyraenidae Barracudas Sphyraena spp. x Trichiuridae Pacific Scabbardfish Lepidopus fitchi x Scombridae Scombrids x Mackerels Auxis spp (9.9) , Skipjack Tuna Katsuwonus pelamis Pacific Chub Mackerel Scomber japonicus 21.4 (3.5) , Balistidae Balistids (triggerfishes) x Finescale Triggerfish Balistes polylepis 4.5 (2.8) Rough Triggerfish Canthidermis maculata 4.5 (0.5) Blunthead Triggerfish Pseudobalistes naufragium 3.2 (0.4) Monacanthidae Scrawled Filefish Aluterus scriptus 9.2 (1.2) Tetraodontidae Oceanic Puffer Lagocephalus lagocephalus 14.9 (5.0) , Bullseye Puffer Sphoeroides annulatus x Diodontidae Balloonfish Diodon holocanthus Unidentified teleosts Unidentified teleost fishes x Reptiles Cheloniidae Olive ridley sea turtle Lepidochelys olivacea x Total x 1, , * , TABLE 5. Isotopic composition (δ 13 Candδ 15 N, ) of Dolphinfish prey collected off the southern Baja California peninsula. Prey type Average Average C:N (number of samples) Group δ 15 N(SD) δ 13 C (SD) ratio (SD) Argonauta cornutus (2) Cephalopods (0.90) (0.31) 4.51 (1.93) Paper nautiluses Argonauta spp. (5) Cephalopods (1.81) (0.55) 3.45 (0.32) Mackerels Auxis spp. (3) Fish (1.27) (0.27) 3.14 (0.07) Finescale Triggerfish (3) Fish (1.59) (2.55) 4.17 (0.93) Jumbo squid (5) Cephalopods (1.78) (1.04) 3.86 (1.05) Deepwater Cornetfish (3) Fish (1.18) (0.55) 3.43 (0.31) Oceanic Puffer (3) Fish (0.39) (0.36) 3.21 (0.11) Red crab (3) Crustaceans 7.95 (1.69) (1.55) 6.44 (1.01) Pacific Sardine (5) Fish (1.49) (1.24) 3.19 (0.12) Bigeye Scad (3) Fish (0.32) (0.24) 3.37 (0.19)

9 FEEDING HABITS AND TROPHIC POSITION OF DOLPHINFISH N C Males (n = 22) Females (n = 26) FIGURE 2. Mean ( ± SD) δ 13 Candδ 15 N values for male and female Dolphinfish collected off the southern Baja California peninsula. values (U = 197.0, P = 0.06) also did not differ significantly between sexes. Mixing model results indicated that the main prey species for Dolphinfish of both sexes was the red crab (Table 6). Comparison of Diet by Size-Class According to the%iri, there were changes in the contribution of each prey species to the diets of Dolphinfish in the different size-classes. The smallest Dolphinfish (<65 cm FL) fed mainly on Pacific Sardine (30%), while the largest individuals (>110 cm FL) fed mainly on jumbo squid (45%; Figure 3). The ANOSIM showed that there was a separation in the diet between the two size-groups (R ANOSIM = 0.15). The H value varied with TABLE 6. Estimated proportional prey inputs (as determined from the Bayesian isotope mixing model, MixSIR) to the diets of male and female Dolphinfish in the waters south of the Baja California peninsula, Mexico (CI = confidence interval). Male Dolphinfish Female Dolphinfish 95% 95% Prey type Median CI Median CI Argonauta cornutus Paper nautiluses Argonauta spp. Mackerels Auxis spp Finescale Triggerfish Jumbo squid Deepwater Cornetfish Oceanic Puffer Red crab Pacific Sardine Bigeye Scad specimen size; the smallest individuals had the highest value (<65 cm: H = 3.50), and the largest individuals had the lowest value (>110 cm: H = 1.32). The Bi values were less than 0.6 for all size-classes (range = ). No relationship was observed between the size of predatory Dolphinfish and the size of fish prey (Spearman s rank correlation analysis: r = 0.008, P = 0.89), crustacean prey (r = 0.043, P = 0.73), or cephalopod prey (r = 0.030, P = 0.89; Figure 4). The δ 13 C muscle values did not significantly differ among Dolphinfish size-classes (Kruskal Wallis ANOVA: H 4, 46 = 5.49, P = 0.24); however, the smallest individuals had higher δ 15 N values than the largest individuals (H 4, 46 = 9.48, P = 0.04; Figure 5). The mixing model results indicated that the relative contribution of red crabs was significantly different among Dolphinfish size-classes (Kruskal Wallis ANOVA: H 4, 46 = 28.34, P = 0.005; Table 7). Trophic position estimated from stomach content analysis showed no significant difference among Dolphinfish size-classes (Kruskal Wallis ANOVA: H 4, 315 = 1.52, P = 0.82), whereas trophic position based on δ 15 N values was significantly different among size-classes (H 4, 46 = 9.48, P = 0.04), with the smallest Dolphinfish exhibiting higher trophic positions and the largest specimens exhibiting lower trophic positions. Comparison of Diet by Year According to the %IRI, the red crab (30%) and jumbo squid (40%) were the most important prey species for Dolphinfish in 2005, whereas the red crab was the most important prey species in both 2006 (75%) and 2007 (65%). An increase in the H value was observed over the study years (2005 H = 1.72; 2006 H = 2.07; 2007 H = 3.17); Bi values were less than 0.6 during all 3 years (2005 Bi = 0.09; 2006 Bi = 0.24; 2007 Bi = 0.14). The ANOSIM showed no diet separation among sampling years (R ANOSIM = 0.03). However, in comparing our results with those of previous studies in the area, interannual changes in Dolphinfish feeding habits were evidenced by variations in the%iri. Dolphinfish fed mainly on fishes and cephalopods during summer in 1990 and 1991 (Aguilar-Palomino et al. 1998), whereas cephalopods and crustaceans were the most important components of the diet during summer in 2000, 2001, and 2003 (Tripp-Valdez et al. 2010) and (present study; Figure 6). No significant variations in stable isotope signatures were observed among sampling years (Kruskal Wallis ANOVA, δ 15 N: H 2, 48 = 1.84, P = 0.39; δ 13 C: H 2, 48 = 1.02, P = 0.59; Figure 7). The mixing model results indicated that the same prey species occurred in the Dolphinfish s diet during all three sampling years (Figure 8); however, Dolphinfish specimens that were caught during 2005 had a higher dietary contribution of red crabs than Dolphinfish that were caught during 2006 and 2007 (Kruskal Wallis ANOVA: H 2, 48 = 27.90, P = 0.005). The mean trophic position values estimated for the different years ranged from 3.8 to 4.0 based on stomach content analysis

10 536 TORRES-ROJAS ET AL. FIGURE 3. Percent index of relative importance (%IRI) calculated for prey types consumed by Dolphinfish of each sex and size-class (cm FL). The number of Dolphinfish examined is indicated above each bar. See Table 4 for common names of prey types. (Kruskal Wallis ANOVA: H 2, 315 = 4.73, P = 0.09) and from 3.6 to 3.7 based on stable isotope analysis (H 2, 48 = 1.81, P = 0.40). DISCUSSION The observed variations in the feeding habits and trophic position of Dolphinfish are critical to understanding the ecology and role of this species in marine ecosystems. These results provide knowledge of feeding locations, seasonal prey utilization, and prey availability and may be helpful in predicting possible ecological responses to environmental change (Hückstädt et al. 2012; Hobday et al. 2013). The trophic spectrum and feeding strategies observed in this study were similar to those previously reported for Dolphinfish off the southern Baja California peninsula (Aguilar-Palomino et al. 1998; Tripp-Valdez 2005), with epipelagic prey species being the primary components of the diet and mesopelagic and bathypelagic species making lesser contributions to the diet. In this study, both stomach content analysis and stable isotope analysis confirmed that the Dolphinfish is a predator that feeds mostly on epipelagic prey species. Dolphinfish had lower δ 15 N values than Pacific Angel Sharks Squatina californica caught in the same area, as the latter species displays benthic feeding habits (δ 15 N = ± 0.27 [mean ± SD]; Escobar-Sánchez et al. 2010). The difference between the two predators is related to the difference in δ 15 N values of primary producers in the epipelagic food chain (5.7 ; White et al. 2007) versus the benthic food chain (9.3 ; Altabet et al. 1999) within the Gulf of California.

11 FEEDING HABITS AND TROPHIC POSITION OF DOLPHINFISH 537 Fish total length (cm) Crustaceans total length (cm) Cephalopods total length (cm) Dolphinfish fork length (cm) Dolphinfish fork length (cm) Dolphinfish fork length (cm) FIGURE 4. Relationship between the fork lengths of predatory Dolphinfish captured off the southern Baja California peninsula and the total lengths of prey from the three main prey groups: (a) prey fish, (b) crustaceans, and (c) cephalopods. The line in each panel represents the linear regression model. The muscle δ 15 N and δ 13 C values indicated that the red crab was the main contributor to the Dolphinfish s diet during summer, but the percent contribution of this prey species was lower than that observed in stomach contents. The importance of the red crab could be related to its high abundance in the waters off the southern Baja California peninsula (Aurioles-Gamboa b c a 15 N C 46-65cm (n = 4) cm (n = 8) cm (n = 11) cm (n = 17) cm (n = 6) FIGURE 5. Mean ( ± SD) δ 13 Candδ 15 N values for five size-classes (cm FL) of Dolphinfish collected off the southern Baja California peninsula. and Pérez-Flores 1995), which is influenced by the California Current during spring and summer (Stevenson 1970). The presence of crustaceans (e.g., Hemisquilla californiensis)in the Dolphinfish s diet has also been reported in other areas of Mexico, including near Mazatlán (Tripp-Valdez et al. 2010), and could be related to high densities that make crustaceans easier to catch. The dietary contributions of fishes and cephalopods as observed from stable isotope analysis were higher than the contributions (i.e.,%iri) calculated from stomach content analysis. The%IRI could be biased by the presence of numerous small prey items (e.g., red crabs) and because identification of the diet based only on an organism s last meal can underestimate the importance of prey items that are easily digested and lack hard parts. In contrast, the stable isotope composition integrates an organism s diet over greater time scales, provides dietary data for individuals with empty digestive tracts, and indicates the relative masses of foods that are actually assimilated (Vander Zanden et al. 1997; O Reilly et al. 2002). Variation in Feeding Habits The high complexity of the feeding habits of larger predatory fishes, which feed at different levels of the food web at different points in their life history, may be influenced by (1) intrinsic factors, such as morphology, size, and mobility; (2) factors related to their prey (e.g., prey availability and abundance); and (3) other external factors (e.g., seasonal and long-term environmental changes; Hart and Ison 1991; Stergiou and Fourtouni 1991; Brewer and Warburton 1992). In this study, we observed no segregation in the Dolphinfish s diet by sex, which agrees with previous reports for the area (Tripp-Valdez et al. 2010). However, size-related differences in feeding strategies particularly between Dolphinfish smaller than 65 cm FL and those larger than 110 cm FL were observed based on stomach content analysis and stable isotope analysis. Other authors have reported that the diets of Dolphinfish vary with body size: small individuals that feed near floating objects in subsurface waters consume abundant crustacean prey, and

12 538 TORRES-ROJAS ET AL. TABLE 7. Estimated proportional prey inputs (as determined from the Bayesian isotope mixing model, MixSIR) to the diets of Dolphinfish by size-class inthe waters south of the Baja California peninsula, Mexico (CI = confidence interval). Dolphinfish size-class (FL) cm cm cm cm cm Prey type Median 95% CI Median 95% CI Median 95% CI Median 95% CI Median 95% CI Argonauta cornutus Paper nautiluses Argonauta spp Mackerels Auxis spp Finescale Triggerfish Jumbo squid Deepwater Cornetfish Oceanic Puffer Red crab Pacific Sardine Bigeye Scad larger individuals preferentially consume cephalopods in offshore areas. These differences have been reported for Dolphinfish in the western Atlantic Ocean off Hatteras, North Carolina (Rose and Hassler 1974); the eastern Caribbean (Oxenford and Hunte 1999); Japanese waters (Sakamoto and Kojima 1999); and the eastern Pacific Ocean (Olson and Galván-Magaña 2002; Tripp-Valdez et al. 2010). Anecdotal information indicates that small Dolphinfish travel together in schools ranging from just a few fish to over 50 individuals, whereas larger Dolphinfish live alone or in pairs. In FIGURE 6. Interannual variation in the feeding habits (% index of relative importance [%IRI]) of Dolphinfish collected off the southern Baja California peninsula. Data are from Aguilar-Palomino (1993; data for 1990 and 1991), Tripp-Valdez (2005; data for 2000, 2001, and 2003), and the present study (data for ). The number of Dolphinfish examined is indicated above each bar. See Table 4 for common names of prey types.

13 FEEDING HABITS AND TROPHIC POSITION OF DOLPHINFISH 539 δ 15 N δ 13 C 2005 (n = 20) 2006 (n = 11) 2007 (n = 17) FIGURE 7. Mean ( ± SD) δ 13 Candδ 15 N values of Dolphinfish collected off the southern Baja California peninsula during each sampling year. our study, the most significant difference in feeding behavior was observed for the smallest (<65 cm) and largest (>110 cm) males, which are known as bull dorado. A transition group composed of cm males and females was also observed. Spatial stratification by size for the purpose of avoiding cannibalism (Hendrix 1983; Uchiyama et al. 1992; Kraul 1993) could explain the variation in diet between the smallest and largest specimens of Dolphinfish. The observed interannual variation in the diets of Dolphinfish between (primarily fishes and cephalopods) and (primarily crustaceans and cephalopods) could be related to faunal displacement events. The causes of such faunal displacements are likely related to the occurrence of the tropical phenomenon of ENSO and its effect on the California Current system (Lluch-Belda et al. 2005). Hubbs (1948) and Wooster (1980) each reported the presence of tropical fish species (e.g., Pacific Chub Mackerel Scomber japonicus) off the California coast in relation to an ENSO event. During , there was an ENSO event that allowed actively swimming species (i.e., fishes) to extend their distributions northward (Lluch-Belda et al. 2005). This could explain the greater presence of fish prey in the Dolphinfish s diet during The fish prey species that were observed in the diets of Dolphinfish for (Aguilar-Palomino et al. 1998) were the same as those reportedly consumed by Dolphinfish specimens caught off the Jalisco coast (south of Cabo San Lucas; Amezcua-Gomez 2007). Thus, northward latitudinal shifts in fauna are seemingly related to warming events. During , a significant decline in the importance of jumbo squid in the Dolphinfish s diet was accompanied by an increased importance of red crabs. The jumbo squid fishery in the central Gulf of California collapsed in 1998 (Actualización de la Carta Nacional Pesquera 2010) after the El Niño (Markaida et al. 2008). The low contribution of jumbo squid to the Dolphinfish s diet in was probably linked to the impact of the 1998 ENSO event, and the decreasing trend observed from 2003 to 2006 was also possibly related to another ENSO event occurring in that period. Therefore, the observed variations in jumbo squid abundance in the Dolphinfish s diet seem to correspond with periods of alternating cold and warm ocean conditions. Nevárez-Martínez et al. (2010) identified a pattern in jumbo squid recruitment variability relative to environmental variability: warmer waters caused by El Niño conditions in the California Current coincided with low recruitment, whereas cooler waters (identified as negative sea surface temperature anomalies) caused by La Niña conditions were related to high recruitment. The red crab is a eurythermic prey species (9 28 C; Longhurst 1967) with a high tolerance for changes in water temperature, which could explain this species dominance in the Dolphinfish s diet during both El Niño and La Niña events. Dolphinfish showed high abundances during El Niño conditions ( ) and low abundances during La Niña conditions ( ), likely due to their preference for warmer waters (Aguilar-Palomino et al. 1998; Tripp-Valdez et al. 2010), leading to their probable departure from the study area during La Niña events. FIGURE 8. Mixing model estimates of prey inputs for Dolphinfish sampled off the southern Baja California peninsula in Sample size is shown above each column. See Table 4 for common names of prey types. Variation in Trophic Position Based on the trophic position estimated using both stomach content analysis and stable isotope analysis ( ), the Dolphinfish occupies a high trophic position and exhibits a high degree of plasticity, being able to occupy different trophic positions from secondary carnivore to tertiary carnivore. In contrast to the results of Olson and Watters (2003), who reported a trophic position of 4.5 for Dolphinfish in the eastern tropical Pacific Ocean, we found a range of values indicating that there was some variation in trophic position. Despite the fact that the Dolphinfish s diet mostly consisted of red crabs, the relative importance of different prey types (occupying different trophic positions) among different size-classes, as already mentioned, could have contributed to the variability in trophic position.