Abstract
The strategies of food partitioning among two abundant estuarine puffer fishes, Sphoeroides greeleyi (Gilbert, 1900) and Sphoeroides testudineus (Linnaeus, 1758), were investigated in a tropical hypersaline estuary. We examined the stomachs of 946 fishes collected with a beach seine across three zones (upper, middle and lower estuary) along with a salinity gradient. The highest abundances of species were recorded in the upper and middle estuary. The diet was comprised mostly by benthic organisms, mainly Bivalvia, Gastropoda, and Brachyura. However, in a hypersaline estuary, these species develop strategies of resource partitioning in three ways: 1) asymmetry effects; 2) habitat selection; and 3) trade-offs among age classes. Diet variations according to fish age classes indicated that the largest individuals showed a decrease in their consumption of small preys (Amphipods, Copepods, and Ceratopogonidae) and an increase in their consumption of larger preys (Bivalvia and Decapoda). This behavior of switching diet towards larger prey was related to the functional trade-offs in swimming capacity, and feeding mode used to capture prey. The middle and upper estuary are important feeding grounds for puffer fishes, as demonstrated by their influence on prey distributions and habitat type. Diet breadth indicated that S. greeleyi tended to be a generalist, whereas S. testudineus tended to be a specialist. Thus, the strategies of partitioning seem to have importance for puffer fish populations in this hypersaline environment.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Álvares CA, Stape JL, Sentelhas PC, Gonçalves JLM, Sparovek G (2014) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26:32–46. https://doi.org/10.1111/j.1442-9993.2001.01070.pp.x
Araújo MS, Bolnick DL, Layman CG (2011) The ecological causes of individual specialization. Ecol Lett 14:948–958. https://doi.org/10.1111/j.1461-0248.2011.01662.x
Araújo PRV, Costa SYL, Duarte MRN, Pessanha ALM (2016) Feeding and spatial distribution of two estuarine puffer fish in a tropical north-eastern Brazil. J Mar Biol Assoc UK:1–8. https://doi.org/10.1017/S0025315416001454
Beaumord AC, Petrere M Jr (1994) Fish communities of Manso River, Chapada dos Guimarães, MT, Brazil. Acta Biol Venez 152:21–35
Boeuf G, Payan P (2001) How should salinity influence fish growth? Comp Biochem Physiol C 130:411–423. https://doi.org/10.1016/S1532-0456(01)00268-X
Brännäs E (2008) Temporal resources partitioning varies with individual competitive ability: a test with artic charr Salvelinus alpinus visiting a feeding site from refuge. J Fish Biol 73:524–535. https://doi.org/10.1111/j.1095-8649.2008.01941.x
Chen Y, Yang Z (2005) Diets of obscure puffer (Takifugu obscurus) and ocellated puffer (Takifugu ocellatus) during spawning migration. J Freshw Ecol 20:195–196. https://doi.org/10.1080/02705060.2005.9664953
Chi-Espínola AA, Vegas-Cendejas ME (2013) Feeding habits of Sphoeroides testudineus (Perciformes: Tetraodontidae) in the lagoon system of ria Lagartos, Yucatán, Mexico. Rev Biol Trop 61:849–856. https://doi.org/10.15517/rbt.v61i2.11229
Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Crow SK, Closs GP, Waters JM, Booker DJ, Wallis GP (2010) Niche partitioning and the effect of interspecific competition on microhabitat use by two sympatric galaxiid stream fishes. Freshw Biol 55:967–982. https://doi.org/10.1111/j.1365-2427.2009.02330.x
Denadai MR, Santos FB, Bessa S, Bernardes LP, Turra A (2012) Population biology and diet of the puffer fish Lagocephalus laevigatus (Tetraodontiformes Tetraodonidae) in Caraguatatuba bay, south-eastern Brazil. J Mar Biol Assoc UK 92:407–412. https://doi.org/10.1017/S0025315411001299
Di Iulio-Ilarri M, Souza AT, Medeiros PR, Grempel RG, Rosa IML (2008) Effect of tourist visitation and supplementary feeding on fish assemblage composition on a tropical reef in the southwestern Atlantic. Neotrop Ichthyol 6:651–656. https://doi.org/10.1590/S1679-62252008000400014
Dias TLP, Rosa RS, Damasceno LCP (2007) Aspectos socioeconômicos, percepção ambiental e perspectivas das mulheres marisqueiras da Reserva de Desenvolvimento Sustentável Ponta do Tubarão (Rio Grande do Norte). Gaia. Scientia 1:25–35
Duncan RS, Szelistowski WA (1998) Influence of puffer predation on vertical distribution of mangrove littorinids in the Gulf of Nicoya, Costa Rica. Oecologia 117:433–442. https://doi.org/10.1007/s004420050678
Elliot M, Whitfield AK, Potter IC, Blaber SJ, Cyrus DP, Nordlie FG, Harrison TD (2007) The guild approach to categorizing estuarine fish assemblages: a global review. Fish Fish 8:241–268. https://doi.org/10.1111/j.1467-2679.2007.00253.x
Fávaro LF, Oliveira EC, Ventura AO, Verani NF (2009) Environmental influences on the spatial and temporal distribution of the puffer fish Sphoeroides greeleyi and Sphoeroides testudineus in Brazilian subtropical estuary. Neotrop Ichthyol 7:275–282. https://doi.org/10.1590/S1679-62252009000200020
Figueiredo JL, Menezes NA (2000) Manual de peixes marinhos do Sudeste do Brasil. VI.Teleostei (5). São Paulo, Museu de Zoologia da Universidade de São Paulo
Gatz, AJ, Jr (1979) Community organization in fishes as indicate by morphological features. Ecology 60: 711–718. https://doi.org/10.2307/1936608
Giacomini HC (2007) Os mecanismos de coexistência de espécies como visto pela teoria ecológica. Oecol Bras 11:521–543. https://doi.org/10.4257/oeco.2007.1104.05
Giarrizzo T, Krumme U, Wosniok W (2010) Size-structured migration and feeding patterns in the banded puffer fish Colomesus psittacus (Tetraodontidae) from north Brazilian mangrove creeks. Mar Ecol Prog Ser 419:157–170. https://doi.org/10.3354/meps08852
Gning N, Le Loc’h F, Thiaw OT, Aliaume C, Vidy G (2010) Estuarine resources use by juvenile Flagfin mojorra (Eucionostomus melanopterus) in an inverse tropical estuarine (sine Saloum, Senegal). Estuar Coast Shelf S 86:683–691. https://doi.org/10.1016/j.ecss.2009.11.037
Gordon MS, Plaut I, Kim D (1996) How puffers (Telostei: Tetraodontidae) swim. J Fish Biol 49:319–328. https://doi.org/10.1111/j.1095-8649.1996.tb00026.x
Guevera E, Sánchez AJ, Rosas C, Mascaró M, Brito R (2007) Asociación trófica de peces distribuídos em vegetación acuática submergida em la Laguna de Términos, sur del Golfo de México. Universidad y. Ciencia 23:151–166. https://doi.org/10.19136/era.a23n2.289
Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93:145–159. https://doi.org/10.1086/282070
Hyslop EJ (1980) Stomach contents analysis – a review of methods and their application. J Fish Biol 17:411–429. https://doi.org/10.1111/j.1095-8649.1980.tb02775.x
Jackson AC, Rundle SD, Atrill MJ, Cotton PA (2004) Ontogenetic changes in metabolism may determine diet shifts for a sit-and-wait predator. J Anim Ecol 73:536–545. https://doi.org/10.1111/j.0021-8790.2004.00831.x
Keast A, Webb D (1966) Mouth and body form relative to feeding ecology in the fish fauna of a small lake, lake Opinicon, Ontario. J Fish Res Board Can 23:1845–1874. https://doi.org/10.1139/f66-175
Kneitel JM, Chase JM (2004) Trade-offs in community ecology: linking spatial scales and species coexistence. Ecol Lett 7:69–80. https://doi.org/10.1046/j.1461-0248.2003.00551.x
Krebs CJ (1999) Ecological methodology. Addison-Wesley Educational Publishers, Inc., New York
Krumme U, Keuthen H, Saint-Paul U, Villwock W (2007) Contribution to the feeding ecology of the banded puffer fish Colomesus psittacus (Tetraodontidae) in north Brazilian mangrove creeks. Braz J Biol 67:383–392. https://doi.org/10.1590/S1519-69842007000300002
Labropoulou M, Eleftheriou A (1997) The foraging ecology of two pairs of congeneric demersal fish species: importance of morphological characteristics in prey selection. J Fish Biol 50:324–340. https://doi.org/10.1111/j.1095-8649.1997.tb01361.x
Loureiro-Crippa VE, Hahnn NS (2006) Use of food resources by the fish fauna of a small reservoir (rio Jordão, Brazil), before and shortly after its filling. Neotrop Ichthyol 4:357–362. https://doi.org/10.1590/S1679-62252006000300007
Mabragana E, Giberto DA, Bremec CS (2005) Feeding ecology of Bathyraja macloviana (Rajiformes: Arhynchobatidae): a polychaete-feeding skate from the south-west Atlantic. Sci Mar 69:405–413. https://doi.org/10.3989/scimar.2005.69n3405
Marian S, Maccaroni A, Massa F, Rampacci M, Tancioni L (2002) Lack of consistency between the tropic interrelationships of five sparid species in two adjacent central Mediterranean coastal lagoons. J Fish Biol 61:138–147. https://doi.org/10.1111/j.1095-8649.2002.tb01767.x
McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82(1):290–297.
Medeiros CRF, Costa AKS, Lima CSS, Oliveira JM, Cavalcanti Júnior MM, Silva MRA, Gouveia RSD, Melo JIM, Dias TLP, Molozzi J (2016) Environmental drivers of the benthic macroinvertebrates community in a hypersaline estuary (northeastern Brazil). Acta Limnol Bras 28:1–8. https://doi.org/10.1590/S2179-975X2815
Mendoza-Carranza M, Vieira JP (2009) Ontogenetic niche feeding partitioning in juvenile of white sea catfish Genidens barbus in estuarine environments, southern Brazil. J Mar Biol Assoc UK 89:839–848. https://doi.org/10.1017/S0025315408002403
Murie DJ (1995) Comparative feeding ecology of two sympatric rockfish congeners Sebastes caurinus (copper rockfish) and S. maliger (quillback rockfish). Mar Biol 124:341–353. https://doi.org/10.1007/BF00363908
Palacios-Sánchez S, Vega-Cendejas ME (2010) Cambios alimentícios em três espécies de Sphoeroides (Tetraodontiformes: Tetraodontidae) posterior al huracán Isidoro en Bocana de la Carbonera, Sureste del Golfo de Mexico. Rev Biol Trop 58:1223–1235. https://doi.org/10.15517/rbt.v58i4.5407
Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL (2006) Distribution and diet of four species of carcharhinid shark in the Hawaian Islands: evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 320:239–251. https://doi.org/10.3354/meps320239
Pessanha ALM, Araújo FG, Oliveira REMCC, Silva AF (2015) Ecomorphology and resource use by dominant species of tropical estuarine juvenile fishes. Neotrop Ichthyol 13:1–12. https://doi.org/10.1590/1982-0224-20140080
Piet GJ (1998) Ecomorphology of a size structured tropical freshwater fish community. Environ Biol Fish 51:67–86. https://doi.org/10.1023/A:1007338532482
Pinkas L, Oliphont MS, Iverson ILK (1971) Food habits of albacore, blue fin tuna and bonito in California waters. Calif Fish Game 152:1–105
Platell ME, Potter IC (2001) Partitioning of food resources amongst 18 abundant benthic carnivorous fish species in marine waters on the lower west coast of Australia. J Exp Mar Biol Ecol 262:31–54. https://doi.org/10.1016/s0022-0981(01)00257-x
Platell ME, Potter IC, Clarke KR (1998) Resource partitioning by four species of elasmobranchs (Batoidea: Urolophidae) in coastal waters of temperate Australia. Mar Biol 131:719–734. https://doi.org/10.1007/s002270050363
Platell ME, Orr PA, Potter IC (2006) Inter- and intraspecific partitioning food resources by six large and abundant fish species in a seasonally open estuary. J Fish Biol 69:243–262. https://doi.org/10.1111/j.1095-8649.2006.01098.x
Platell ME, Hesp SA, Cossington SM, Lek E, Moore SE, Potter IC (2010) Influence of selected factors on three dietary compositions of three targeted and co-occurring temperate species of reef fishes: implications for food partitioning. J Fish Biol 76:1255–1276. https://doi.org/10.1111/j.1095-8649.2010.02537.x
Plaut I, Chen SA (2003) How small puffers (Telostei: Tetraodontidae) swim. Ichthyol Res 50:149–153. https://doi.org/10.1007/s10228-002-0153-3
Potter IC, Chuwen BM, Hoeksema SD, Elliott M (2010) The concept of an estuary: a definition that incorporates systems which can become closed to the ocean and hypersaline. Estuar Coast Shelf S 87:497–500. https://doi.org/10.1016/j.ecss.2010.01.021
Prodocimo V, Freire CA (2004) Estuarine pufferfishes (Sphoeroides testudineus and S. greeleyi) submitted to sea water dilution during ebb tide: a field experiment. Mar Fresw Behav Phy 37:1–5. https://doi.org/10.1080/10236240310001603765
Prodocimo V, Freire CA (2006) The Na+, K+, 2Cl− cotransporter of estuarine pufferfishes (Sphoeroides testudineus and S. greeleyi) in hypo- and hyper-regulation of plasma osmolality. Comp Biochem Physiol C 142:347–355. https://doi.org/10.1016/j.cbpc.2005.11.013
Prodocimo V, Souza CF, Pessini C, Fernandes LC, Freire CA (2008) Metabolic substrates are not mobilized from the osmoregulatory organs (gill and kidney) of the estuarine pufferfishes Sphoeroides greeleyi and S. testudineus upon short-term salinity reduction. Neotrop Ichthyol 6:613–620. https://doi.org/10.1590/S1679-62252008000400009
Queiroz RNM, Dias TLP (2014) Molluscs associated with the macroalgae of the genus Gracilaria (Rhodophyta): importance of algal fronds as microhabitat in a hypersaline mangrove in northeastern Brazil. Braz J Biol 74:52–63. https://doi.org/10.1590/1519-6984.20712
Quevedo M, Svanbäck R, Eklöv P (2009) Intrapopulation niche partitioning in a generalist predator limits food web connectivity. Ecology 90:2263–2274. https://doi.org/10.1890/07-1580.1
Ralston KR, Wainwright PC (1997) Functional consequences of trophic specialization in pufferfishes. Funct Ecol 11:43–52. https://doi.org/10.1046/j.1365-2435.1997.00057.x
Rocha C, Favaro LF, Spach HL (2002) Biologia reprodutiva de Sphoeroides testudineus (Linnaeus) (Pisces, Osteichthyes, Tetraodontidae) da gamboa do Baguaçu, Baía de Paranaguá, Paraná, Brasil. Rev Bras Zool 19:57–63. https://doi.org/10.1590/S0101-81752002000100003
Ross ST (1986) Resource partitioning in fish assemblages: a review of field studies. Copeia 2:352–388. https://doi.org/10.2307/1444996
Russo T, Pulcini D, O’Leary A, Cataudella S, Mariani S (2008) Relationship between body shape and trophic niche segregation in two closely related sympatric fishes. J Fish Biol 73:809–828. https://doi.org/10.1111/j.1095-8649.2008.01964.x
Sales NS, Dias TLP, Baeta A, Pessanha ALM (2016) Dependence of juvenile reef fishes on semi-arid hypersaline estuary microhabitats as nurseries. J Fish Biol 89:661–679. https://doi.org/10.1111/jfb.13006
Santos ACA, Rodriguez FNC (2011) Ocorrência e alimentação do baiacu Sphoeroides testudineus (Actinopterygii – Tetraodontiformes) na margem oeste da Baía de Todos os Santos, Bahia, Brasil. Sitientibus série Ciências Biológicas 11(1):31–36. https://doi.org/10.13102/scb11
Savenije HHG (2006) Salinity and tides in alluvial estuaries. Elsevier Science, Amsterdam
Schaefer KM (1992) An evaluation of geographic and annual variation in morfometric characters and gill-raker counts of yellowfin tuna, Thunnus albacares, from the Pacific ocean. Inter-American Tropical Tuna Commission. Special Report 20:135–163
Schafer LNM, Platell E, Potter IC, Valesini FJ (2002) Comparisons between the influence of habitat type, season and body size on the dietary compositions of fish species in nearshore marine waters. J Exp Mar Biol Ecol 278:67–92. https://doi.org/10.1016/S0022-0981(02)00337-4
Schoener TW (1974) Resource partitioning in ecological communities. Science 185:27–39. https://doi.org/10.1126/science.185.4145.27
Schultz YD, Favaro LF, Spach HL (2002) Reproductive aspects of Sphoeroides greeleyi (Gilbert), Tetraodontidae, from gamboa do Baguaçu, Paranaguá, state of Paraná, Brazil. Rev Bras Zool 19:65–76. https://doi.org/10.1590/S0101-81752002000100004
Silva RS, Carvalho KD, Pessanha ALM (2016) Distribution and feed ecology of three juvenile mojarras in a hypersaline tropical estuary in northeastern Brazil. Mar Ecol 37:1266–1281. https://doi.org/10.1111/maec.12316
Simier M, Blanc L, Aliaume C, Diouf PS, Albaret JJ (2004) Spatial and temporal structure of fish assemblages in an “inverse estuary” the sine Saloum system (Senegal). Estuar Coast Shelf S59:69–86. https://doi.org/10.1016/j.ecss.2003.08.002
Sommerville E, Platell ME, White WT, Jones AA, Potter IC (2011) Partitioning of food resources by four abundant, co-occurring elasmobranch species and the relationships between diet and season, body size, region and feeding mode. Mar Freshw Res 62:54–65. https://doi.org/10.1071/MF10164
Targett TE (1978) Food resource partitioning by the pufferfishes Sphoeroides spengleri and S. testudineus from Biscayne Bay, Florida. Mar Biol 49:83–91. https://doi.org/10.1007/BF00390732
Turigan RG (1994) Ecomorphological relationships among Caribbean tetraodontiform fishes. J Zool (Lond) 233:493–521. https://doi.org/10.1111/j.1469-7998.1994.tb05279.x
Van Wassenbergh S, Herrel A, Adriaens D, Aerts P (2007) No trade-off between biting and suction feeding performance in clariid catfishes. J Exp Biol 210:27–36. https://doi.org/10.1242/jeb.02619
Vega-Cendejas MA, de Santillana MH (2004) Fish community structure and dynamics in a coastal hypersaline lagoon: Rio Lagartos, Yucatan, Mexico. Estuar Coast Shelf S 60:285–299. https://doi.org/10.1016/j.ecss.2004.01.005
Verdiell-Cubedo D, Oliva-Paterna FJ, Ruiz-Navarro A, Torralva M (2013) Assessing the nursery role for marine fish species in a hypersaline coastal lagoon (mar Menor, Mediterranean Sea). Mar Biol Res 00:1–11. https://doi.org/10.1080/17451000.2013.765580
Wainwright PC, Richard BA (1995) Predicting patterns of prey use from morphology of fishes. Environ Biol Fish 44(1-3):97–113. https://doi.org/10.1007/BF00005909
Watson DJ, Balon EK (1984) Ecomorphological analysis of fish taxocenes in rainforest streams of northern Borneo. J Fish Biol 25:371–383. https://doi.org/10.1111/j.1095-8649.1984.tb04885.x
Werner EE, Gilliam JF (1984) The ontogenetic niche and species interactions in size-structured populations. Annu Rev Ecol Syst 15:393–425. https://doi.org/10.1146/annurev.es.15.110184.002141
White WT, Platell ME, Potter IC (2004) Comparisons between the diets of four abundant species of elasmobranchs in a subtropical embayment: implications for resource partitioning. Mar Biol 144:439–448. https://doi.org/10.1007/s00227-003-1218-1
Yamahira K, Kikuchi T, Nojima S (1996) Age specific food utilization and spatial distribution of the puffer, Takifugu niphobles, over an intertidal sand flat. Environ Biol Fish 45:311–318. https://doi.org/10.1007/BF00003100
Yan M, Li Z, Xiong B, Zhu J (2004) Effects of salinity on food intake, growth, and survival of pufferfish (Fugu obscurus). J Appl Ichthyol 20:146–149. https://doi.org/10.1046/j.1439-0426.2003.00512.x
Yan M, Li Z, Xiong B (2005) Preliminary results on osmolality response of pufferfish Takifugu obscurus* to sudden salinity change. J Appl Ichthyol 21:156–159. https://doi.org/10.1111/j.1439-0426.2004.00589.x
Yang Z, Chen YF (2008) Differences in reproductive strategies between obscure puffer Takifugu obscurus and ocellated puffer Takifugu ocellatus during their spawning migration. J Appl Ichthyol 24:569–573. https://doi.org/10.1111/j.1439-0426.2008.01071.x
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
da Silva Lima, C.S., Clark, F.J.K., Sales, N.S. et al. Strategies of resource partitioning between two sympatric puffer fishes in a tropical hypersaline estuary, Brazil. Environ Biol Fish 101, 1105–1119 (2018). https://doi.org/10.1007/s10641-018-0729-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-018-0729-z