A negative trade-off between current reproductive effort and reproductive success: an experiment with clutch-size in a tropical bird
Nadinni O. M. Sousa A C and Miguel Â. Marini B
+ Author Affiliations
- Author Affiliations
A Programa de Pós-graduação em Biologia Animal, Instituto de Ciências Biológicas, Universidade de Brasília, 70910-900, Brasília, DF, Brazil.
B Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade de Brasília, 70910-900, Brasília, DF, Brazil.
C Corresponding author. Present address: Departamento de Áreas Protegidas, Secretaria de Biodiversidade e Florestas, Ministério do Meio Ambiente, 70068-900, Brasília, DF, Brazil. Email: nadinni.sousa@mma.gov.br
Emu 113(1) 8-18 https://doi.org/10.1071/MU11102
Submitted: 20 December 2011 Accepted: 4 September 2012 Published: 27 November 2012
Abstract
Clutch-size is thought to be the result of a trade-off between current reproductive effort, which may be constrained by current food supply, and current and future reproductive success. Studying the selective pressures that determine clutch-size is crucial for understanding life-history strategies. In order to examine how the costs associated with increasing energy demands during reproduction affect reproductive success, we experimentally manipulated clutch-sizes of Lesser Elaenia (Elaenia chiriquensis) in the Brazilian Cerrado. This species has a clutch-size of two, the most common clutch-size for tropical birds. We manipulated nests to create artificial clutches of one and three eggs. We tested if nestling survival and growth, risk of nest predation and incubation efficiency in larger clutches influenced reproductive success, and how parents responded to these demands in food provisioning and incubation behaviour. Neither clutch-size nor nestling age affected nest predation or incubation efficiency, but parental activity did increase with increased clutch-size and increasing age of nestlings. However, growth of nestlings was negatively influenced by increasing clutch-size, which is likely to affect both the quantity and quality of young produced. Our data show that parental investment during the nestling stage may be a key factor in the evolution of small clutch-sizes in tropical birds.
Additional keywords: clutch manipulation, Elaenia chiriquensis, evolution of clutch-size, food provisioning, incubation effort, life-history strategies, Neotropical savanna, nest-predation risk, parental care.
References
Alves, M. A. S. (1991). Dieta e táticas de forrageamento de Neothraupis fasciata em cerrado no Distrito Federal, Brasil (Passeriformes : Emberizidae). Revista Brasileira de Ornitologia 2, 25–29.Amaral, M. F., and Macedo, R. H. F. (2003). Breeding patterns and habitat use in the endemic Curl-crested Jay of central Brazil. Journal of Field Ornithology 74, 331–340.
Auer, S. K., Bassar, R. D., Fontaine, J. J., and Martin, T. E. (2007). Breeding biology of passerines in a subtropical montane forest in northwestern Argentina. Condor 109, 321–333.
| Breeding biology of passerines in a subtropical montane forest in northwestern Argentina.Crossref | GoogleScholarGoogle Scholar |
Both, C., Visser, M. E., and Verboven, N. (1999). Density-dependent recruitment rates in Great Tits: the importance of being heavier. Proceedings of the Royal Society of London B – Biological Sciences 266, 465–469.
| Density-dependent recruitment rates in Great Tits: the importance of being heavier.Crossref | GoogleScholarGoogle Scholar |
Bretz, F., Hothorn, T., and Westfall, P. (2011). ‘Multiple Comparisons using R.’ (CRC Press: Boca Raton, FL.)
Burnham, K. P., and Anderson, D. R. (2002). ‘Model Selection and Multimodel Inference: A Practical Information–Theoretic Approach.’ (Springer: New York.)
Cichón, M. (2000). Cost of incubation and immunocompetence in the Collared Flycatcher. Oecologia 125, 453–457.
| Cost of incubation and immunocompetence in the Collared Flycatcher.Crossref | GoogleScholarGoogle Scholar |
Cody, M. L. (1966). A general theory of clutch size. Evolution 20, 174–184.
| A general theory of clutch size.Crossref | GoogleScholarGoogle Scholar |
Conway, C. J., and Martin, T. E. (2000a). Effects of ambient temperature on avian incubation behavior. Behavioral Ecology 11, 178–188.
| Effects of ambient temperature on avian incubation behavior.Crossref | GoogleScholarGoogle Scholar |
Conway, C. J., and Martin, T. E. (2000b). Evolution of passerine incubation behavior: influence of food, temperature, and nest predation. Evolution 54, 670–685.
| 1:STN:280:DC%2BD3cvgtlKqug%3D%3D&md5=17cfd411a848b0baed4e2d42b939e4a7CAS |
Dias, R. I., and Macedo, R. H. (2011). Nest predation versus resources in a Neotropical passerine: constraints of the food limitation hypothesis. Ornis Fennica 88, 30–39.
Dijkstra, C., Bult, A., Bijlsma, S., Daan, S., Meijer, T., and Zijlstra, M. (1990). Brood size manipulations in the Kestrel (Falco tinnunculus): effects on offspring and parent survival. Journal of Animal Ecology 59, 269–285.
| Brood size manipulations in the Kestrel (Falco tinnunculus): effects on offspring and parent survival.Crossref | GoogleScholarGoogle Scholar |
Dobbs, R. C., Styrsky, J. D., and Thompson, C. F. (2006). Clutch size and the cost of incubation in the House Wren. Behavioral Ecology 17, 849–856.
| Clutch size and the cost of incubation in the House Wren.Crossref | GoogleScholarGoogle Scholar |
dos Santos, L. R., and Marini, M. Â. (2010). Breeding biology of the White-rumped Tanager (Cypsnagra hirundinacea) in central Brazil. Journal of Field Ornithology 81, 252–258.
| Breeding biology of the White-rumped Tanager (Cypsnagra hirundinacea) in central Brazil.Crossref | GoogleScholarGoogle Scholar |
Duca, C., and Marini, M. Â. (2011). Variation in breeding of the Shrike-like Tanager in central Brazil. Wilson Journal of Ornithology 123, 259–265.
| Variation in breeding of the Shrike-like Tanager in central Brazil.Crossref | GoogleScholarGoogle Scholar |
Engstrand, S. M., and Bryant, D. M. (2002). A trade-off between clutch size and incubation efficiency in the Barn Swallow Hirundo rustica. Functional Ecology 16, 782–791.
| A trade-off between clutch size and incubation efficiency in the Barn Swallow Hirundo rustica.Crossref | GoogleScholarGoogle Scholar |
Ferretti, V., Llambías, P. E., and Martin, T. E. (2005). Life-history variation of a Neotropical thrush challenges food limitation theory. Proceedings of the Royal Society of London B – Biological Sciences 272, 769–773.
| Life-history variation of a Neotropical thrush challenges food limitation theory.Crossref | GoogleScholarGoogle Scholar |
Fontaine, J. J., and Martin, T. E. (2006). Parent birds assess nest predation risk and adjust their reproductive strategies. Ecology Letters 9, 428–434.
| Parent birds assess nest predation risk and adjust their reproductive strategies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD283jsFKmsw%3D%3D&md5=b07a8fb1c376e96f6a802c8ef0f89202CAS |
Fontaine, J. J., Martel, M., Markland, H. M., Niklison, A. M., Decker, K. L., and Martin, T. E. (2007). Testing ecological and behavioral correlates of nest predation. Oikos 116, 1887–1894.
| Testing ecological and behavioral correlates of nest predation.Crossref | GoogleScholarGoogle Scholar |
França, L. C., and Marini, M. Â. (2009). Teste do efeito de borda na predação de ninhos naturais e artificiais no cerrado do Planalto Central, Brasil. Revista Brasileira de Zoologia 26, 241–250.
França, L. F., Sousa, N. O. M., dos Santos, L. R., Duca, C., Gressler, D. T., Borges, F. J. A., Lopes, L. E., Manica, L. T., Paiva, L. V., Medeiros, R. C. S., and Marini, M. Â. (2009). Passeriformes: nest predators and prey in a Neotropical savannah in central Brazil. Zoologia 26, 799–802.
Francisco, M. R. (2006). Breeding biology of the Double-collared Seedeater (Sporophila caerulescens). Wilson Journal of Ornithology 118, 85–90.
| Breeding biology of the Double-collared Seedeater (Sporophila caerulescens).Crossref | GoogleScholarGoogle Scholar |
Ghalambor, C. K., and Martin, T. E. (2002). Comparative manipulation of predation risk in incubating birds reveals the variability in the plasticity of responses. Behavioral Ecology 13, 101–108.
| Comparative manipulation of predation risk in incubating birds reveals the variability in the plasticity of responses.Crossref | GoogleScholarGoogle Scholar |
Grieco, F. (2001). Short-term regulation of food-provisioning rate and effect on prey size in Blue Tits, Parus caeruleus. Animal Behaviour 62, 107–116.
| Short-term regulation of food-provisioning rate and effect on prey size in Blue Tits, Parus caeruleus.Crossref | GoogleScholarGoogle Scholar |
Grieco, F. (2002). How different provisioning strategies result in equal rates of food delivery: an experimental study of Blue Tits Parus caeruleus. Journal of Avian Biology 33, 331–341.
| How different provisioning strategies result in equal rates of food delivery: an experimental study of Blue Tits Parus caeruleus.Crossref | GoogleScholarGoogle Scholar |
Gustafsson, L., and Sutherland, W. J. (1988). The costs of reproduction in the Collared Flycatcher Ficedula albicollis. Nature 335, 813–815.
| The costs of reproduction in the Collared Flycatcher Ficedula albicollis.Crossref | GoogleScholarGoogle Scholar |
Hatchwell, B. J., Russell, A. F., MacColl, A. D. C., Ross, D. J., Fowlie, M. K., and McGowan, A. (2004). Helpers increase long-term but not short-term productivity in cooperatively breeding Long-tailed Tits. Behavioral Ecology 15, 1–10.
| Helpers increase long-term but not short-term productivity in cooperatively breeding Long-tailed Tits.Crossref | GoogleScholarGoogle Scholar |
Heaney, V., and Monaghan, P. (1996). Optimal allocation of effort between reproductive phases: the trade-off between incubation costs and subsequent brood rearing capacity. Proceedings of the Royal Society of London B – Biological Sciences 263, 1719–1724.
| Optimal allocation of effort between reproductive phases: the trade-off between incubation costs and subsequent brood rearing capacity.Crossref | GoogleScholarGoogle Scholar |
Hoi, H., Kristin, A., Valera, F., and Hoi, C. (2004). Clutch enlargement in Lesser Gray Shrikes (Lanius minor) in Slovakia when food is superabundant: a maladaptive response? Auk 121, 557–564.
| Clutch enlargement in Lesser Gray Shrikes (Lanius minor) in Slovakia when food is superabundant: a maladaptive response?Crossref | GoogleScholarGoogle Scholar |
Hõrak, P. (2003). When to pay the cost of reproduction? A brood size manipulation experiment in Great Tits (Parus major). Behavioral Ecology and Sociobiology 54, 105–112.
Hothorn, T., Bretz, F., Westfall, P., Heiberger, R. M., and Schützenmeister, A. (2011). Multcomp: Simultaneous Inference in General Parametric Models. R package version 1.2–7. (R Foundation for Statistical Computing: Vienna, Austria.)
Ilmonen, P., Taarna, T., and Hasselquist, D. (2002). Are incubation costs in female Pied Flycatchers expressed in humoral immune responsiveness or breeding success? Oecologia 130, 199–204.
Lebreton, J. D., Burnham, K. P., Clobert, J., and Anderson, D. R. (1992). Modeling survival and testing biological hypothesis using marked animals: a unified approach with case studies. Ecological Monographs 62, 67–118.
| Modeling survival and testing biological hypothesis using marked animals: a unified approach with case studies.Crossref | GoogleScholarGoogle Scholar |
Lindèn, M., and Moller, A. P. (1989). Cost of reproduction and covariation of life history traits in birds. Trends in Ecology & Evolution 4, 367–371.
| Cost of reproduction and covariation of life history traits in birds.Crossref | GoogleScholarGoogle Scholar |
Lopes, L. E., and Marini, M. Â. (2005). Low reproductive success of Campo Suiriri (Suiriri affinis) and Chapada Flycatcher (S. islerorum) in the central Brazilian Cerrado. Bird Conservation International 15, 337–346.
| Low reproductive success of Campo Suiriri (Suiriri affinis) and Chapada Flycatcher (S. islerorum) in the central Brazilian Cerrado.Crossref | GoogleScholarGoogle Scholar |
MacColl, A. D. C., and Hatchwell, B. J. (2003). Sharing of caring: nestling provisioning behaviour of Long-tailed Tit, Aegithalos caudatus, parents and helpers. Animal Behaviour 66, 955–964.
| Sharing of caring: nestling provisioning behaviour of Long-tailed Tit, Aegithalos caudatus, parents and helpers.Crossref | GoogleScholarGoogle Scholar |
Marini, M. Â., and Cavalcanti, R. B. (1990). Migrações de Elaenia albiceps chilensis e Elaenia chiriquensis albivertex (Aves, Tyrannidae). Boletim do Museu Paraense Emílio Goeldi 6, 59–66.
Martin, T. E. (1987). Food as a limit on breeding birds: a life-history perspective. Annual Review of Ecology and Systematics 18, 453–487.
| Food as a limit on breeding birds: a life-history perspective.Crossref | GoogleScholarGoogle Scholar |
Martin, T. E. (1992). Interaction of nest predation and food limitation in reproductive strategies. Current Ornithology 9, 163–197.
Martin, T. E. (1995). Avian life history evolution in relation to nest sites, nest predation, and food. Ecological Monographs 65, 101–127.
| Avian life history evolution in relation to nest sites, nest predation, and food.Crossref | GoogleScholarGoogle Scholar |
Martin, T. E. (2002). A new view for avian life-history evolution tested on a incubation paradox. Proceedings of the Royal Society of London B – Biological Sciences 269, 309–316.
| A new view for avian life-history evolution tested on a incubation paradox.Crossref | GoogleScholarGoogle Scholar |
Martin, T. E. (2004). Avian life-history evolution has an eminent past: does it have a bright future? Auk 121, 289–301.
| Avian life-history evolution has an eminent past: does it have a bright future?Crossref | GoogleScholarGoogle Scholar |
Martin, T. E., Martin, P. R., Oslon, C. R., Heidinger, B. J., and Fontaine, J. J. (2000a). Parental care and clutch sizes in North and South American birds. Science 287, 1482–1485.
| Parental care and clutch sizes in North and South American birds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsV2qt7c%3D&md5=4e6cf9ca25d9cde18a6878aa5213e09bCAS |
Martin, T. E., Scott, J., and Menge, C. (2000b). Nest predation increases with parental activity: separating nest site and parental activity effects. Proceedings of the Royal Society of London B – Biological Sciences 267, 2287–2293.
| Nest predation increases with parental activity: separating nest site and parental activity effects.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MzltFSltg%3D%3D&md5=8111f3eb53a9d8e935a4df85f60bd063CAS |
Martin, T. E., Bassar, R. D., Bassar, S. K., Fontaine, J. J., Lloyd, P., Mathewson, H. A., Niklison, A. M., and Chalfoun, A. (2006). Life-history and ecological correlates of geographic variation in egg and clutch mass among passerine species. Evolution 60, 390–398.
Medeiros, R. C. S., and Marini, M. Â. (2007). Biologia reprodutiva de Elaenia chiriquensis (Lawrence) (Aves, Tyrannidae) em cerrado do Brasil Central. Revista Brasileira de Zoologia 24, 12–20.
| Biologia reprodutiva de Elaenia chiriquensis (Lawrence) (Aves, Tyrannidae) em cerrado do Brasil Central.Crossref | GoogleScholarGoogle Scholar |
Monaghan, P., and Nager, R. G. (1997). Why don’t birds lay more eggs? Trends in Ecology & Evolution 12, 270–274.
| Why don’t birds lay more eggs?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7itFKruw%3D%3D&md5=23f60166a3fb6294e72b91f27ec3a5edCAS |
Monaghan, P., Nager, R. G., and Houston, D. C. (1998). The price of eggs: increased investment in egg production reduces offspring rearing capacity of parents. Proceedings of the Royal Society of London B – Biological Sciences 265, 1731–1735.
| The price of eggs: increased investment in egg production reduces offspring rearing capacity of parents.Crossref | GoogleScholarGoogle Scholar |
Muchai, M., and du Plessis, M. A. (2005). Nest predation of grassland bird species increases with parental activity at the nest. Journal of Avian Biology 36, 110–116.
| Nest predation of grassland bird species increases with parental activity at the nest.Crossref | GoogleScholarGoogle Scholar |
Murphy, M. T. (2000). Evolution of clutch size in the Eastern Kingbird: tests of alternative hypotheses. Ecological Monographs 70, 1–20.
| Evolution of clutch size in the Eastern Kingbird: tests of alternative hypotheses.Crossref | GoogleScholarGoogle Scholar |
Nilsson, J. A., and Seversson, E. (1996). The cost of reproduction: a new link between current reproductive effort and future reproductive success. Proceedings of the Royal Society of London B – Biological Sciences 263, 711–714.
| The cost of reproduction: a new link between current reproductive effort and future reproductive success.Crossref | GoogleScholarGoogle Scholar |
Paiva, L. V. (2008). Fatores que determinam o período reprodutivo de Elaenia chiriquensis (Aves:Tyrannidae) no Cerrado do Brasil Central. Ph.D. Thesis, Universidade de Brasília, Brazil.
Pettifor, R. A., Perrins, C. M., and McCleery, R. H. (1988). Individual optimization of clutch size in Great Tits. Nature 336, 160–162.
| Individual optimization of clutch size in Great Tits.Crossref | GoogleScholarGoogle Scholar |
Pinheiro, J., and Bates, D. DebRoy, S., and Sarkar, D. (2006). nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1–78. (R Foundation for Statistical Computing: Vienna, Austria.)
R Development Core Team (2006). ‘R: a language and Environment for Statistical Computing.’ (R Foundation for Statistical Computing: Vienna, Austria.) Available at http://www.R-project.org [Verified 10 October 2012].
Reid, J. M., Monaghan, P., and Ruxton, G. D. (2000a). The consequences of clutch size for incubation conditions and hatching success in Starlings. Functional Ecology 14, 560–565.
| The consequences of clutch size for incubation conditions and hatching success in Starlings.Crossref | GoogleScholarGoogle Scholar |
Reid, J. M., Monaghan, P., and Ruxton, G. D. (2000b). Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation. Proceedings of the Royal Society of London B – Biological Sciences 267, 37–41.
| Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7jsVCisg%3D%3D&md5=69e895f670a8348afb649a8322c9f09aCAS |
Ricklefs, R. E. (2000). Density dependence, evolutionary optimization, and the diversification of avian life histories. Condor 102, 9–22.
| Density dependence, evolutionary optimization, and the diversification of avian life histories.Crossref | GoogleScholarGoogle Scholar |
Roper, J. J. (2005). Try and try again: nest predation favors persistence in a Neotropical bird. Ornitologia Neotropical 16, 253–262.
Roper, J. J., and Goldstein, R. R. (1997). A test of the Skutch hypothesis: does activity at nests increase nest predation risk? Journal of Avian Biology 28, 111–116.
| A test of the Skutch hypothesis: does activity at nests increase nest predation risk?Crossref | GoogleScholarGoogle Scholar |
Sick, H. (1997). ‘Ornitologia Brasileira.’ (Nova Fronteira: Rio de Janeiro, Brazil.)
Skutch, A. F. (1949). Do tropical birds rear as many birds as they can nourish? Ibis 91, 430–455.
| Do tropical birds rear as many birds as they can nourish?Crossref | GoogleScholarGoogle Scholar |
Skutch, A. F. (1985). Clutch size, nesting success, and predation on nests of Neotropical birds, reviewed. Ornithological Monographs 36, 575–593.
Slagsvold, T. (1982). Clutch size variation in passerine birds: the nest predation hypothesis. Oecologia 54, 159–169.
| Clutch size variation in passerine birds: the nest predation hypothesis.Crossref | GoogleScholarGoogle Scholar |
Slagsvold, T. (1984). Clutch size variation of birds in relation to nest predation: on the cost of reproduction. Journal of Animal Ecology 53, 945–953.
| Clutch size variation of birds in relation to nest predation: on the cost of reproduction.Crossref | GoogleScholarGoogle Scholar |
Stutchbury, B. J. M., and Morton, E. S. (2001). ‘Behavioral Ecology of Tropical Birds.’ (Academic Press: San Diego, CA.)
Stutchbury, B. J. M., and Morton, E. S. (2008). Recent advances in the behavioral ecology of tropical birds. Wilson Journal of Ornithology 120, 26–37.
| Recent advances in the behavioral ecology of tropical birds.Crossref | GoogleScholarGoogle Scholar |
Styrsky, J. N., Brawn, J. D., and Robinson, S. K. (2005). Juvenile mortality increases with clutch size in a Neotropical bird. Ecology 86, 3238–3244.
| Juvenile mortality increases with clutch size in a Neotropical bird.Crossref | GoogleScholarGoogle Scholar |
Tarwater, C. E., Kelley, J. P., and Brawn, J. D. (2009). Parental response to elevated begging in a high predation, tropical environment. Animal Behaviour 78, 1239–1245.
| Parental response to elevated begging in a high predation, tropical environment.Crossref | GoogleScholarGoogle Scholar |
Tarwater, C. E., Ricklefs, R. E., Maddox, J. D., and Brawn, J. D. (2011). Pre-reproductive survival in a tropical bird and its implications for avian life histories. Ecology 92, 1271–1281.
| Pre-reproductive survival in a tropical bird and its implications for avian life histories.Crossref | GoogleScholarGoogle Scholar |
Visser, M. E., and Lessells, C. M. (2001). The costs of egg production and incubation in Great Tits (Parus major). Proceedings of the Royal Society of London B – Biological Sciences 268, 1271–1277.
| The costs of egg production and incubation in Great Tits (Parus major).Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mzkslyktg%3D%3D&md5=d27113e1a754f3fe84477b00e1bc954eCAS |
White, G. C., and Burnham, K. P. (1999). Program MARK: survival estimation from populations of marked animals. Bird Study 46, S120–S139.
| Program MARK: survival estimation from populations of marked animals.Crossref | GoogleScholarGoogle Scholar |
Williams, G. C. (1966). Natural selection, the costs of reproduction, and a refinement of Lack’s principle. American Naturalist 100, 687–690.
| Natural selection, the costs of reproduction, and a refinement of Lack’s principle.Crossref | GoogleScholarGoogle Scholar |
Williams, J. B. (1996). Energetics of avian incubation. In ‘Avian Energetics and Nutritional Ecology’. (Ed. C. Carey.) pp. 375–416. (Chapman and Hall: New York.)
Young, B. E. (1996). An experimental analysis of small clutch size in tropical house wrens. Ecology 77, 472–488.
| An experimental analysis of small clutch size in tropical house wrens.Crossref | GoogleScholarGoogle Scholar |
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., and Smith, G. M. (2009). ‘Mixed Effects Models and Extensions in Ecology with R.’ (Springer: New York.)