SciELO - Scientific Electronic Library Online

 
vol.45 número5First record of Parasphaerosyllis indica (Polychaetae: Syllidae) from Easter Island, ChileAvances en el estudio reproductivo de la reineta (Brama australis) en la costa central de Chile índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • En proceso de indezaciónCitado por Google
  • No hay articulos similaresSimilares en SciELO
  • En proceso de indezaciónSimilares en Google

Compartir


Latin american journal of aquatic research

versión On-line ISSN 0718-560X

Lat. Am. J. Aquat. Res. vol.45 no.5 Valparaíso nov. 2017

http://dx.doi.org/10.3856/vol45-issue5-fulltext-24 

Short Communication

Characterizing trophic ecology of the checkered puffer (Sphoeroides testudineus)

Ryann E. Rossi1 

Sean T. Giery1  2 

Erika W. Bonnema1 

Allison L. Todd1 

Craig A. Layman1 

1Department of Applied Ecology, North Carolina State University, Raleigh, USA

2Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, USA

ABSTRACT

Sphoeroides testudineus (Linnaeus, 1758), is a common, widely distributed fish in coastal ecosystems. To better understand the trophic niche of S. testudineus, we collected individuals from tidal creeks on Abaco Island, The Bahamas, and employed stomach content and stable isotope analysis. Examination of stomach contents showed that mollusks, such as West Indian false cerith snails, cerith snails, and tellin clams, were the most common prey items. Diet data were consistent with stable isotopes data such that S. testudineus seem to feed at an intermediate trophic position in the food web. These preliminary data suggest that S. testudineus may be a critical intermediate link in these wetland food webs, serving as pathways through which energy is transferred from primary consumers to other predator species.

Keywords: Sphoeroides testudineus; diet; food web; mangrove; predator-prey; stable isotopes

Checkered puffers, Sphoeroides testudineus (Linnaeus, 1758), are a common inhabitant of coastal habitats along the eastern United States and throughout the Caribbean (Pauly, 1991; MacDonald et al., 2009; Thiem et al., 2013). S. testudineus are common foragers within intertidal areas, often following rising tides to feed. Despite their extensive geographic range, broad habitat use, abundance, and foraging habits, there are relatively few dietary data for this species. Here, we use stomach content data and stable isotopes (δ13C and δ15 N) to examine the trophic ecology of S. testudineus from Abaco island, The Bahamas. We first address diet composition of S. testudineus and the diet of major consumed taxa. Finally, we use previously collected isotope data to offer qualitative comparisons among other common tidal creek fishes to better understand their relative role in tidal creek food webs.

Our study focused on two ecologically similar tidal creeks on Abaco Island: Broad Creek (BC: 26°29'28.23”N, 77°2'40.86”W) and Sandy Point (SP: 26°0'31.05”N, 77°24'8.04”W). Both tidal creeks are fringed by dwarf red mangrove (Rhizophora mangle) and have benthic habitats consisting of seagrasses (primarily Thalassia testudinum), green macroalgae (Batophora oerstedii, Halimeda discoidea, Acetebularia spp.), and barren sand flats (Araújo et al., 2014; Chacín et al., 2015). To assess the taxonomic composition of S. testudineus diets we examined the stomach contents of 11 fish from BC and 15 from SP. Fish were captured with traps and hook-and-line in July 2014. Stomach contents were identified to the lowest taxonomic resolution possible (usually to genus) and volume of each prey item determined by water displacement following Winemiller (1990). Unidentified prey was grouped as shell fragments or unidentified tissue.

Tissue samples (muscle) for isotope analysis were collected from each fish. Samples were dried at 60°C for 48 h, ground to fine powder, and analyzed at the stable isotope/Soil Biology Laboratory at University of Georgia, Athens, GA. Source contributions to prey were estimated as consumer-specific means of posterior distributions generated in SIAR (Fig. 1a). Trophic discrimination values were set at 3.4‰ δ15N and 1‰ δ13C for S. testudineus prey following Post (2002). Isotope values (prey, and primary producers: T. testudinum, R. mangle, and B. oerstedii) included samples collected from Abaco tidal creeks.

Figure 1 a) Proportion of three resource pools that may support prey of pooled S. testudineus samples was based on simple stable isotope mixing models among - red mangrove (R. mangle; orange), batophora (B. oerstedii; green), and turtlegrass (T. testudinum; blue). The isotope signatures for basal resources were inputted to models as: red mangrove (n = 129, δ13C = -25.7, SD ± 1.5 and δ15N = -0.9, ± 3.8), batophora (n = 18, δ13C = -18.7, ± 3.4 and δ15N = -1.9, ± 1.2), and turtlegrass (n = 25, δ13C = -10.1, ± 1.4 and δ15N = 0.1, ± 2.0), b) comparison of δ13C and δ15N values between S. testudineus and other common species in the sampled creek systems. Error bars are standard deviations. 

For a community-level understanding of S. testudineus trophic ecology in our study system, we use previously collected (from 2009) isotope data for a range of fish species often coexisting with S. testudineus in Bahamian tidal creeks (Layman et al., 2004). Given that these data were not collected at the same time, and often from different tidal creek systems, we do not offer a quantitative comparison of trophic position. Rather, we simply display these data together with pufferfish prey to highlight areas of dietary overlap among these common fishes.

Our stomach content analysis showed that S. testudineus diet was composed of ten benthic invertebrate taxa, the vast majority of which are mollusks (Tellin clams, Batillaria and Cerith snails; Table 1), and to a lesser extent, crustaceans. However, there were some obvious differences between sites. For example, SP fish consumed more Tellin clams (63%), and fewer Batillaria snails (38%) than BC fish. BC fish also consumed taxa associated with mangroves: Littorina anguilfera, Aratus pisonii, Brachidontes exustus, and Amphibalanus amphitrite, while SP fish did not (Table 1). This bias towards mangrove consumers in BC pufferfish may explain the slightly more depleted δ13C signatures they exhibit (BC = -17.1 ± 1.1, SP = -15.4 ± 1.4). Indeed, isotope data show that prey taxa rely on different combinations of basal resource pools (Fig. 1a). For example, L. anguilfera (arboreal grazers) shows the most depleted δ13C values (δ13C = -22‰), suggesting strong trophic linkages to red mangrove-derived carbon (δ13C -25.7, Fig. 1a). At the opposite compositional extreme, Cerith snails (benthic herbivores) showed the most enriched δC13 values (δ13C = -11.6‰), suggesting strong reliance on seagrass-derived carbon (δ13C = -10.1, Fig. 1a). Nevertheless, most prey taxa seemed to incorporate moderate-to-low amounts of mangrove-derived carbon which is not surprising given that most species are primarily benthic grazers or filter-feeders.

Table 1 The proportion of prey items by volume in S. testudineus diets from each tidal creek. The proportion of prey items was calculated by dividing the sum of the volume of each prey type by the sum of the volume of all prey items in the diet of each individual specimen. 

Taxa Stomach contents Isotope values
Broad creek (BC) Sandy point (SP) n δ13C δ15N
West Indian false cerith Batillaria minima 37.9 8.9 10 -16.7 2.6
Striped barnacle Amphibalanus amphitrite 13.6 2 -13.7 3.8
Nerite snail Nerita spp. 11.6 1.8 9 -18.3 3.1
Cerith snail Cerith spp. 8.2 22.6 29 -11.6 2.4
Mangrove periwinkle Littorina anguilfera 8.0 3 -22.0 0.9
Scorched mussel Brachidontes exustus 7.8 0.7 11 -13.8 2.7
Algae 5.8 3.3
Mangrove tree crab Aratus pisonii 3.7
Tellin clam Tellin spp. 3.4 62.8 4 -16.2 2.8
Amphipod Amphipoda 0.1

While there was substantial interspecific variation in resource pools used by the various prey taxa, there is little variation in the δ15N axis among the prey taxa assessed (mean δ15N = 2.6 ‰), again suggesting that all feed primarily on basal resources.

To help change to illustrate general food web structure in these systems, we provide stable isotope values for other species common in tidal creek systems on Abaco (Layman et al., 2007, Layman & Allgeier, 2012; Araújo et al., 2014; Giery & Layman, 2015). We find that S. testudineus appears to occupy an intermediate trophic position, like common benthic invertivores such as yellowfin mojarra (Gerres cinereus), schoolmaster snapper (Lutjanus apodus), and grey snapper (L. griseus; Fig. 1b). Our data also suggest relatively high fractionation rate of δ15N (~5‰) between the two main prey items (Tellin spp. and Batillaria spp.) and S. testudineus. This is slightly greater than the mean reported fractionation rate of 3.4‰ (Post 2002). However, there is often variation in fractionation rates. For example, any single trophic transfer could range between 2-5‰ (Post, 2002). It is also possible that S. testudineus consumed higher trophic level prey in time periods earlier than we sampled.

S. testudineus diets are almost exclusively composed of small gastropods and bivalves in Bahamian tidal creeks, which is like S. testudineus diets from Brazil, the Yucatan and Florida (Targett, 1978; Barros et al., 2010; Chi-Espínola & Vega-Cendejas, 2013). S. testudineus from the Brazil sites relied more on gastropods than bivalves, similar to S. testudineus from the BC tidal creek in our study. Macrophytes and Brachyuran crabs also composed a large portion of S. testudineus diet in the Yucatan and Florida, respectively. The apparent preference of benthic mollusks such as Tellin clams and Battilaria snails in Bahamas tidal creeks might be related to their high abundance in these systems (Valentine-Rose et al., 2007).

As predators, they feed on durable, well-protected prey such as mollusks and gastropods, an abundant resource unavailable to many other fishes. S. testudineus also forage in upper reaches of intertidal habitats on rising tides, accessing prey that other aquatic consumers cannot. In general, we know less about S. testudineus as prey. Presumably defended by powerful tetrodotoxins and their unique inflating antipredator behavior, pufferfish appear unlikely to be widely consumed. Their use of shallows and hypersaline habitats may also alleviate predation risk to some degree (Rypel et al., 2007). Nevertheless, documented predators include herons (Ardeidae) and other bony fishes (Randall, 1967; Recher & Recher, 1968). And it is reasonable to expect larger consumers such as juvenile lemon sharks that also enter tidal creeks to feed on S. testudineus (Murchie et al., 2010). In these ways, S. testudineus may act as a unique and under-appreciated link in shallow coastal food webs and their trophic role deserves further study.

ACKNOWLEDGEMENTS

We would like to thank Friends of The Environment, S. Buhler, and H. Levenson for field and lab assistance. This project was funded by NSF GRFP (DGE-0946818) and NSF RAPID (OCE 1541637).

REFERENCES

Araújo, M.S., R.B. Langerhans, S.T. Giery & C.A. Layman. 2014. Ecosystem fragmentation drives increased diet variation in an endemic livebearing fish of The Bahamas. Ecol. Evol., 4: 3298-3308. [ Links ]

Barros, J.C.N., J. de Arruda-Francisco, A.L. Vasconcelos-Filho & D.d.O. Tenorio. 2010. Moluscos encontrados no trato digestivo de Sphoeroides testudineus (Linnaues, 1758) (Teleostei: Tetradontida), no canal de Santa Cruz, Itamraca-Pernambuco, Brasil. Rev. Bras. Engenh. Pesca, 5: 70-80. [ Links ]

Chacín, D.H., S.T. Giery, L.A. Yeager, C.A. Layman & R.B. Langerhans. 2015. Cómo afecta la fragmentación hidrológico comunidades de aves costeras? Un estudio de la isla de Abaco, Bahamas. Wetl. Ecol. Manage., 23: 551-557. [ Links ]

Chi-Espínola, A.A. & M.E. Vega-Cendejas. 2013. Hábitos alimenticios de Sphoeroides testudineus (Perciformes: Tetraodontidae) en el sistema lagunar de Ría Lagartos, Yucatán, México. Rev. Biol. Trop., 61: 849-858. [ Links ]

Giery, S.T. & C.A. Layman. 2015. Interpopulation variation in a condition-dependent signal: predation regime affects signal intensity and reliability. Am. Nat., 186: 187-195. [ Links ]

Layman, C.A. & J.E. Allgeier. 2012. Characterizing trophic ecology of generalist consumers: a case study of the invasive lionfish in The Bahamas. Mar. Ecol. Prog. Ser., 448: 131-141. [ Links ]

Layman, C.A., D.A. Arrington, R.B. Langerhans & B.R. Silliman. 2004. Degree of fragmentation affects fish assemblage structure in Andros Island (Bahamas) estuaries. Caribb. J. Sci., 40: 232-244. [ Links ]

Layman, C.A., J.P. Quattrochi, C.M. Peyer, J.E. Allgeier & K. Suding. 2007. Niche width collapse in a resilient top predator following ecosystem fragmentation. Ecol. Lett., 10: 937-944. [ Links ]

MacDonald, J.A., S. Shahrestani & J.S. Weis. 2009. Behavior and space utilization of two common fishes within Caribbean mangroves: implications for the protective function of mangrove habitats. Estuar. Coast. Shelf Sci., 84: 192-201. [ Links ]

Murchie, K.J., E. Schwager, S.J. Cooke, A.J. Danylchuk, S.E. Danylchuk, T.L. Goldberg, C.D. Suski & D.P. Philipp. 2010. Spatial ecology of juvenile lemon sharks (Negaprion brevirostris) in tidal creeks and coastal waters of Eleuthera, The Bahamas. Environ. Biol. Fish., 89: 95-104. [ Links ]

Pauly, D. 1991. Growth of the checkered puffer Sphoeroides testudineus: postscript to papers by Targett and Pauly & Ingles. Fishbyte, 9: 19-22. [ Links ]

Post, D.M. 2002. Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology, 83: 703-718. [ Links ]

Randall, J.E. 1967. Food habits of reef fishes of the West Indies. Stud. Trop. Oceanogr., 5: 665-847. [ Links ]

Recher, H.F. & J.A. Recher. 1968. Comments on the escape of prey from avian predators. Ecology, 49: 560-562. [ Links ]

Rypel, A.L., C.A. Layman & D.A. Arrington. 2007. Water depth modifies relative predation risk for a motile fish taxon in Bahamian tidal creeks. Estuar. Coast., 30(3): 1-8. [ Links ]

Targett, T.E. 1978. Food resource partitioning by the pufferfishes Sphoeroides spengleri and S. testudineus from Biscayne Bay, Florida. Mar. Biol., 49: 83-91. [ Links ]

Thiem, J.D., C. Hatry, J.W. Brownscombe, F. Cull, A.D. Shultz, A.J. Danylchuk & S.J. Cooke. 2013. Evaluation of radio telemetry to study the spatial ecology of checkered puffers (Sphoeroides testudineus) in shallow tropical marine systems. Bull. Mar. Sci., 89: 559-569. [ Links ]

Valentine-Rose, L., J.A. Cherry, J.J. Culp & K.E. Perez. 2007. Floral and faunal differences between fragmented and unfragmented Bahamian tidal creeks. Wetlands, 27: 702-718. [ Links ]

Winemiller, K.O. 1990. Spatial and temporal variation in tropical fish trophic networks. Ecol. Monogr., 60: 331-367. [ Links ]

Received: October 10, 2016; Accepted: August 10, 2017

Corresponding author: Ryann E. Rossi (rerossi@ncsu.edu)

Corresponding editor: Diego Giberto

Creative Commons License This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License, which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.