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Feeding ecology and life-history strategy of nesting males in a fish with long parental care, Lusitanian toadfish (Halobatrachus didactylus, Batrachoididae)

Published online by Cambridge University Press:  08 July 2015

P.M. Félix ,
M.C.P. Amorim ,
T.J. Pereira ,
P.J. Fonseca ,
C. Sousa-Santos  and
J.L. Costa
P.M. Félix*
Affiliation:
Faculdade de Ciências, MARE – Marine and Environmental Sciences Centre, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal
M.C.P. Amorim
Affiliation:
MARE – Marine and Environmental Sciences Centre, ISPA – Instituto Universitário, Rua Jardim do Tabaco 34, 1149-041 Lisboa, Portugal
T.J. Pereira
Affiliation:
Faculdade de Ciências, MARE – Marine and Environmental Sciences Centre, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal Departamento de Biologia, Escola de Ciências e Tecnologia, Universidade de Évora, Largo dos Colegiais 2, 7004-516 Évora, Portugal
P.J. Fonseca
Affiliation:
Departamento de Biologia Animal, Centro de Biologia Ambiental, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal
C. Sousa-Santos
Affiliation:
MARE – Marine and Environmental Sciences Centre, ISPA – Instituto Universitário, Rua Jardim do Tabaco 34, 1149-041 Lisboa, Portugal
J.L. Costa
Affiliation:
Faculdade de Ciências, MARE – Marine and Environmental Sciences Centre, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal Departamento de Biologia Animal, Centro de Biologia Ambiental, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal
*
Correspondence should be addressed to:P.M. Félix, Faculdade de Ciências, MARE – Marine and Environmental Sciences Centre, Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal Email: pmfelix@fc.ul.pt
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Abstract

The Lusitanian toadfish, Halobatrachus didactylus, like other batrachoidids, is a benthic fish species with nesting behaviour during the breeding season. During this prolonged period it engages in mating activities and remains in the nest providing parental care. It is not known whether males feed while providing parental care but it is likely that their limited mobility may restrict their diet and influence their fitness. As a consequence, egg cannibalism could occur as a life-history strategy. The aim of the present study is to ascertain the feeding behaviour of nesting males, in comparison to mature non-nesting males, and to identify potential life-history traits related to egg cannibalism. Nest-holders were sampled from artificial nests placed in an intertidal area of the Tagus estuary, only exposed during spring low tides. The diet of nest-holders was compared with that of non-nesting mature males from the same area, captured by otter trawl. The present study demonstrates that despite their constrained mobility nest-holders feed during the breeding season, although in a more opportunistic fashion than non-nesting males. Nest-holders showed a generalist feeding behaviour, with a more heterogeneous diet. Egg cannibalism was not related to male condition, paternity or brood size but showed a higher incidence early in the season when water temperatures were lower. The results suggest a possible seasonal trade-off strategy between care and energy recovery, triggered by environmental factors, where under unfavourable conditions to sustain viable eggs the male may recover energy by eating eggs, thus benefiting future reproductive success, later in the season.

Keywords

Stomach contentsopportunistic feedingnest-holdersbreeding seasonegg cannibalismenergy trade-offtemperature influencerainfall influenceTagus estuary
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 3 , May 2016 , pp. 657 - 665
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Amorim, M.C.P., Simões, J.M. and Fonseca, P.J. (2008) Acoustic communication in the Lusitanian toadfish, Halobatrachus didactylus: evidence for an unusual large vocal repertoire. Journal of the Marine Biological Association of the United Kingdom 88, 1069–1073.Google Scholar
Arnaud, P. and Hureau, J.-C. (1966) Régime alimentaire de trois téléostéens Nototheniidae antarctiques (Terre Adélie). Bulletin de l'Institut Océanographique de Mónaco 66, 1–24.Google Scholar
Arora, H.L. (1948) Observations on the habits and early life history of the batrachoid fish, Porichthys notatus Girard. Copeia 1948, 89–93.Google Scholar
Barimo, J.F., Serafy, J.E., Frezza, P.E. and Walsh, P.J. (2007) Field studies on the Gulf toad-fish Opsanus beta: habitat utilization, urea production and spawning. Marine Biology 150, 495–508.Google Scholar
Bass, A.H., Horvath, B.J. and Brothers, E.B. (1996) Nonsequential developmental trajectories lead to dimorphic vocal circuitry for males with alternative reproductive tactics. Journal of Neurobiology 30, 493–504.Google Scholar
Bauchot, M.L. (1987) Poissons osseux. In Fischer, W., Schneider, M. and Bauchot, M.-L. (eds) Fiches FAO D'identification des Espèces Pour les Besoins de la Pêche. Mediterranée et Mer Noire (Zone de Pêche 37). Revision 1, Volume II-Vertebrés. Rome: FAO, pp. 891–1421.Google Scholar
Belles-Isles, J.C. and Fitzgerald, G.J. (1991) Filial cannibalism in sticklebacks: a reproductive management strategy. Ethology, Ecology and Evolution 3, 49–62.Google Scholar
Campos, M.C., Costa, J.L., Quintella, B.R., Costa, M.J. and Almeida, P.R. (2008) Activity and movement patterns of the Lusitanian toadfish inferred from pressure-sensitive dataloggers in the Mira estuary (Portugal). Fisheries Management and Ecology 15, 449–458.Google Scholar
Cárdenas, S. (1977) Régimen alimenticio del sapo, Halobatrachus didactylus (Schneider, 1801) (Pisces: Batrachoididae), en la Bahía de Cádiz (España sudoccidental). Vie et Milieu 28, 111–129.Google Scholar
Carriço, R., Amorim, M.C.P. and Fonseca, P.J. (2014) Reproductive success in the Lusitanian toadfish Halobatrachus didactylus: influence of male and nest sizes. Journal of Experimental Marine Biology and Ecology 456, 65–69.Google Scholar
Costa, J.L. (2004) A biologia do xarroco Halobatrachus didactylus (Bloch & Schneider, 1801) e o seu papel na estrutura e funcionamento dos ecossistemas em que se insere; referência especial à população do estuário do Mira. PhD thesis. University of Lisbon, Lisbon, Portugal.Google Scholar
Costa, J.L., Almeida, P.R. and Costa, M.J. (2003) A morphometric and meristic investigation of Lusitanian toadfish Halobatrachus didactylus (Bloch & Schneider, 1801): evidence of population fragmentation on Portuguese coast. Scientia Marina 67, 219–231.Google Scholar
Costa, J.L. and Costa, M.J. (2002) Distribution and abundance of the Lusitanian toadfish, Halobatrachus didactylus (Bloch & Schneider, 1801), in Portugal with some remarks on its population fragmentation. Revista de Biologia 20, 155–167.Google Scholar
Costa, J.L., Domingos, I., Almeida, A.J., Feunteun, E. and Costa, M.J. (2008) Interaction between Halobatrachus didactylus and Anguilla anguilla: what happens when these species occur in sympatry? Cybium 32, 111–117.Google Scholar
Costa, J.L., Silva, G., Almeida, P.R. and Costa, M.J. (2000) Activity and diet of Halobatrachus didactylus (Bloch & Schneider, 1801) adults in the Tagus estuary. Thalassas 16, 21–25.Google Scholar
Costa, M.J. (1999) O Estuário do Tejo. Lisbon: Edições Cotovia.Google Scholar
Cotter, J.C., Pereira, T.J., Costa, M.J. and Costa, J.L. (2013) Distribution, abundance, population structure and activity of Halobatrachus didactylus in the Tagus estuary (Portugal) and adjacent coastal waters. Journal of the Marine Biological Association of the United Kingdom 93, 1–8.Google Scholar
Gomagano, D. and Kohda, M. (2008) Partial filial cannibalism enhances initial body condition and size in paternal care fish with strong male–male competition. Annales Zoologici Fennici 45, 55–65.Google Scholar
Gray, S.M., Dill, L.M. and McKinnon, J.S. (2007) Cuckoldry incites cannibalism: male fish turn to cannibalism when perceived certainty of paternity decreases. American Naturalist 169, 258–263.Google Scholar
Greenfield, D.W., Winterbottom, R. and Collette, B.B. (2008) Review of the toadfish genera (Teleostei: Batrachoididae). Proceedings of the California Academy of Sciences 59, 665–710.Google Scholar
Gross, M.R. and Sargent, R.C. (1985) The evolution of male and female parental care in fishes. American Zoologist 25, 807–822.Google Scholar
Hastie, L.C., Pierce, G.J., Wang, J., Bruno, I., Moreno, A., Piatkowski, U. and Robin, J.-P. (2009) Cephalopods in the north-east Atlantic: species, biogeography, ecology, exploitation and conservation. Oceanography and Marine Biology: An Annual Review 47, 111–190.Google Scholar
Hoffman, S.G. and Robertson, D.R. (1983) Foraging and reproduction of two Caribbean Reef toadfishes (Batrachoididae). Bulletin of Marine Science 33, 919–927.Google Scholar
Hyslop, E.J. (1980) Stomach contents analysis: a review of methods and their application. Journal of Fish Biology 17, 411–429.Google Scholar
Klug, H. and Bonsall, M.B. (2007) When to care for, abandon, or eat your offspring: the evolution of parental care and filial cannibalism. American Naturalist 170, 886–901.Google Scholar
Kvarnemo, C. (1997) Food affects the potential reproductive rates of sand goby females but not of males. Behavioral Ecology 8, 605–611.Google Scholar
Lindström, K. and Sargent, R.C. (1997) Food access, brood size and filial cannibalism in the fantail darter, Etheostoma flabellare. Behavioral Ecology and Sociobiology 40, 107–110.Google Scholar
Lissaker, A., Kvarnemo, C. and Svensson, O. (2003) Effects of a low oxygen environment on parental effort and filial cannibalism in the male sand goby, Pomatoschistus minutus. Behavioral Ecology 14, 374–381.Google Scholar
Manica, A. (2002) Filial cannibalism in teleost fish. Biological Reviews 77, 261–277.Google Scholar
Manica, A. (2003) The effect of brood size and age on partial filial cannibalism in the scissortail sergeant. Journal of Fish Biology 63, 37–47.Google Scholar
Manica, A. (2004) Parental fish change their cannibalistic behaviour in response to the cost-to-benefit ratio of parental care. Animal Behaviour 67, 1015–1021.Google Scholar
Mehlis, M., Bakker, T.C.M., Engqvist, L. and Frommen, J.G. (2010) To eat or not to eat: egg-based assessment of paternity triggers fine-tuned decisions about filial cannibalism. Proceedings of the Royal Society B: Biological Sciences 277, 2627–2635.Google Scholar
Mehlis, M., Bakker, T.C.M. and Frommen, J.G. (2009) Nutritional benefits of filial cannibalism in three-spined sticklebacks (Gasterosteus aculeatus). Naturwissenschaften 96, 399–403.Google Scholar
Modesto, T. and Canário, V.M. (2003) Morphometric changes and sex steroid levels during the annual reproductive cycle of the Lusitanian toadfish, Halobatrachus didactylus. General and Comparative Endocrinology 131, 220–231.Google Scholar
Neff, B.D. (2003) Paternity and condition affect cannibalistic behaviour in nest-tending bluegill sunfish. Behavioral Ecology and Sociobiology 54, 377–384.Google Scholar
Neff, B.D., Repka, J. and Gross, M.R. (2000) Parentage analysis with incomplete sampling of candidate parents and offspring. Molecular Ecology 9, 515–528.Google Scholar
Neff, B.D. and Sherman, P.W. (2005) In vitro fertilization reveals offspring recognition via self- referencing in a fish with paternal care and cuckoldry. Ethology 111, 425–438.Google Scholar
Pereira, T.J., Silva, G., Costa, M.J. and Costa, J.L. (2011) Life strategies of Halobatrachus didactylus (Bloch and Schneider, 1801) in the Tagus estuary: comparison among different morphotypes. Estuarine, Coastal and Shelf Science 93, 328–335.Google Scholar
Ramos, A., Fonseca, P.J., Modesto, T., Almada, V.C. and Amorim, M.C.P. (2012) Alloparental behaviour in the highly vocal Lusitanian toadfish. Journal of Experimental Marine Biology and Ecology 434–435, 58–62.Google Scholar
Robertson, D.R. (1987) Responses of two coral reef toadfishes (Batrachoididae) to the demise of their primary prey, the sea urchin Diadema antillarum. Copeia 3, 637–642.Google Scholar
Rohwer, S. (1978) Parent cannibalism of offspring and egg raiding as a courtship strategy. American Naturalist 112, 429–440.Google Scholar
Sargent, R.C. (1988) Paternal care and egg survival both increase with clutch size in the fathead minnow, Pimephales promelas. Behavioral Ecology and Sociobiology 23, 33–38.Google Scholar
Sargent, R.C. (1992) Ecology of filial cannibalism in fish: theoretical perspective. In Elgar, M.A. and Crespi, B.J. (eds) Cannibalism: ecology and evolution among diverse taxa. Oxford: Oxford University Press, pp. 38–62.Google Scholar
Shannon, C.E. and Weaver, W. (1963) The mathematical theory of communication. Urbana, IL: University of Illinois Press.Google Scholar
Sisneros, J.A., Alderks, P.W., Leon, K. and Sniffer, B. (2009) Morphometric changes associated with the reproductive cycle and behaviour of the interidal-nesting, male plainfin midshipman fish, Porichthys notatus. Journal of Fish Biology 74, 18–36.Google Scholar
Sobral, D. (1981) Contribuição para o estudo da ictiofauna bentónica do estuário do Rio Sado. Licenciature thesis. Faculty of Sciences of the University of Lisbon, Lisbon, Portugal.Google Scholar
Sousa-Santos, C., Fonseca, P.J. and Amorim, M.C.P. (2015) Development and characterization of novel microsatellite loci for Lusitanian toadfish, Halobatrachus didactylus. PeerJ 3, e731. doi: 10.7717/peerj.731.Google Scholar
Svensson, O., Lissäker, M. and Mobley, K.B. (2010) Offspring recognition and the influence of clutch size on nest fostering among male sand gobies, Pomatoschistus minutus. Behavioral Ecology and Sociobiology 64, 1325–1331.Google Scholar
Tokeshi, M. (1991) Graphical analysis of predator feeding strategy and prey importance. Freshwater Forum 1, 179–183.Google Scholar
Vasconcelos, R.O., Carriço, R., Ramos, A., Modesto, T., Fonseca, P.J. and Amorim, M.C.P. (2012) Vocal behaviour predicts reproductive success in a teleost fish. Behavioural Ecology 23, 375–383.Google Scholar
Vasconcelos, R.O., Simões, J.M., Almada, V.C., Fonseca, P.J. and Amorim, M.C.P. (2010) Vocal behaviour during territorial intrusions in the Lusitanian toadfish: boatwhistles also function as territorial ‘keep-out’ signals. Ethology 116, 155–165.Google Scholar
Wilson, C.A., Dean, J.M. and Radtke, R. (1982) Age, growth rate and feeding habits of the oyster toadfish, Opsanus tau (Linnaeus) in South Carolina. Journal of Experimental Marine Biology and Ecology 62, 251–259.Google Scholar