INTRODUCTION: Male contribution to parental care varies widely among avian species. Yet the reasons for this variation, as well as its consequences, are still unclear. Because the amount of care provided by one sex is ultimately constrained by the time available for energy acquisition, contribution by the other sex should increase when overall parental workload is high. We tested this prediction by analyzing male contribution to incubation in 528 populations of 320 species of passerines, where females usually devote more time to incubation than males. Our worldwide sample included species with female-only parental care (the male is not present), incubation feeding (the male feeds the incubating female), and shared incubation (both sexes incubate the eggs). RESULTS: Overall nest attentiveness was greatest in species with shared incubation followed by species with incubation feeding and lowest in species with female-only care. Nest attentiveness and the degree of male contribution to incubation in species with shared incubation were very strongly correlated, whereas this correlation was absent in females. Interestingly, female contribution decreased towards the equator while male contribution did not change significantly with latitude. Hence, relative male incubation effort increased towards the equator, whereas that of female decreased. In species with incubation feeding, female nest attentiveness increased with the frequency of male feeding. CONCLUSIONS: These findings support the hypothesis that male help is indispensable for increasing nest attentiveness in birds, either in the form of incubation feeding (supply of energy) or direct incubation of eggs. We conclude that energy acquisition constraints might be a potent force driving sex-specific contribution to parental care.

Department of Zoology and Laboratory of Ornithology Palacký University 17 listopadu 50 Olomouc 77146 Czech Republic

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Royle NJ, Smiseth PT, Kolliker M. Evolution of Parental Care. Oxford: Oxford University Press; 2012.

Reynolds JD, Goodwin NB, Freckleton RP. Evolutionary transitions in parental care and live bearing in vertebrates. Philos Trans R Soc Lond B Biol Sci. 2002;357:269–281. doi: 10.1098/rstb.2001.0930. PubMed DOI PMC

Gilbert JDJ, Manica A. Parental care trade-offs and life-history relationships in insects. Am Nat. 2010;176:212–226. doi: 10.1086/653661. PubMed DOI

Duellman WE, Trueb L. Biology of Amphibians. New York: McGraw-Hill; 1986.

Mank JE, Promislow DEL, Avise JC. Phylogenetic perspectives in the evolution of parental care in ray-finned fishes. Evolution. 2005;59:1570–1578. PubMed

Cockburn A. Prevalence of different modes of parental care in birds. Proc R Soc London B Biol Sci. 2006;273:1375–1383. doi: 10.1098/rspb.2005.3458. PubMed DOI PMC

Webb TJ, Olson VA, Székely T, Freckleton RP. Who cares? Quantifying the evolution of division of parental effort. Methods Ecol Evol. 2010;1:221–230.

Adrian O, Brockmann I, Hohoff C, Sachser N. Paternal behaviour in wild guinea pigs: a comparative study in three closely related species with different social and mating systems. J Zool. 2005;265:97–105. doi: 10.1017/S0952836904006090. DOI

Balshine S. In: Evolution of Parental Care. Royle NJ, Smiseth PJ, Kolliker M, editor. Oxford: Oxford University Press; 2012. Patterns of Parental Care in Vertebrates; pp. 62–80.

Trumbo S. In: Evolution of Parental Care. Royle NJ, Smiseth PT, Kolliker M, editor. Oxford: Oxford University Press; 2012. Patterns of Parental Care in Invertebrates; pp. 81–100.

Kokko H, Jennions MD. Parental investment, sexual selection and sex ratios. J Evol Biol. 2008;21:919–948. doi: 10.1111/j.1420-9101.2008.01540.x. PubMed DOI

Harrison F, Barta Z, Cuthill I, Székely T. How is sexual conflict over parental care resolved? A meta-analysis. J Evol Biol. 2009;22:1800–1812. doi: 10.1111/j.1420-9101.2009.01792.x. PubMed DOI

Thomson DL, Monaghan P, Furness RW. The demands of incubation and avian clutch size. Biol Rev. 1998;73:293–304. doi: 10.1017/S0006323198005180. DOI

Tinbergen JM, Williams JB. In: Avian Incubation: Behavior, Environment and Evolution. Deeming DC, editor. Oxford: Oxford University Press; 2002. Energetics of Incubation; pp. 298–313.

Reid JM, Monaghan P, Nager RG. In: Avian Incubation: Behavior, Environment and Evolution. Deeming DC, editor. Oxford: Oxford University Press; 2002. Incubation and the Costs of Reproduction; pp. 314–325.

Chalfoun AD, Martin TE. Latitudinal variation in avian incubation attentiveness and a test of the food limitation hypothesis. Anim Behav. 2007;73:579–585. doi: 10.1016/j.anbehav.2006.09.010. DOI

Ueda K. Successive nest building and polygyny of Fan-tailed Warblers Cisticola juncidis. Ibis. 1984;126:221–229.

Di Giacomo AS, Di Giacomo AG, Reboreda JC. Male and female reproductive success in a threatened polygynous species: the strange-tailed tyrant, Alectrurus risora. Condor. 2011;113:619–628. doi: 10.1525/cond.2011.100067. DOI

Bodrati A, Cockle KL. Nesting of the Scalloped Woodcreeper (Lepidocolaptes falcinellus) Ornithol Neotrop. 2011;22:195–206.

Martin TE, Ghalambor CK. Males feeding females during incubation. I. Required by microclimate or constrained by nest predation? Am Nat. 1999;153:131–139. doi: 10.1086/303153. PubMed DOI

Matysioková B, Cockburn A, Remeš V. Male incubation feeding in songbirds responds differently to nest predation risk across hemispheres. Anim Behav. 2011;82:1347–1356. doi: 10.1016/j.anbehav.2011.09.018. DOI

Skutch AF. The incubation patterns of birds. Ibis. 1957;99:69–93.

Deeming DC. Avian Incubation: Behavior, Environment and Evolution. Oxford: Oxford University Press; 2002.

Queller DC. Why do females care more than males? Proc R Soc London B Biol Sci. 1997;264:1555–1557. doi: 10.1098/rspb.1997.0216. DOI

Santos ESA, Nakagawa S. The costs of parental care: a meta-analysis of the trade-off between parental effort and survival in birds. J Evol Biol. 2012;25:1911–1917. doi: 10.1111/j.1420-9101.2012.02569.x. PubMed DOI

Matysioková B, Remeš V. Faithful females receive more help: the extent of male parental care during incubation in relation to extra-pair paternity in songbirds. J Evol Biol. 2013;26:155–162. doi: 10.1111/jeb.12039. PubMed DOI

Weiner J. Physiological limits to sustainable energy budgets in birds and mammals: Ecological implications. Trends Ecol Evol. 1992;7:384–388. doi: 10.1016/0169-5347(92)90009-Z. PubMed DOI

Jeschke JM, Tollrian R. Predicting herbivore feeding times. Ethology. 2005;111:187–206. doi: 10.1111/j.1439-0310.2004.01052.x. DOI

Martin TE. A new view of avian life-history evolution tested on an incubation paradox. Proc R Soc London B Biol Sci. 2002;269:309–316. doi: 10.1098/rspb.2001.1879. PubMed DOI PMC

Russell EM. Extended parental care and delayed dispersal: northern, tropical, and southern passerines compared. Behav Ecol. 2004;15:831–838. doi: 10.1093/beheco/arh088. DOI

Martin TE, Auer SK, Bassar RD, Niklison AM, Lloyd P. Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution. 2007;61:2558–2569. doi: 10.1111/j.1558-5646.2007.00204.x. PubMed DOI

Hammond KA, Diamond J. Maximal sustained energy budgets in humans and animals. Nature. 1997;386:457–462. doi: 10.1038/386457a0. PubMed DOI

Houston AI, Székely T, McNamara JM. Conflict between parents over care. Trends Ecol Evol. 2005;20:33–38. doi: 10.1016/j.tree.2004.10.008. PubMed DOI

McNamara JM, Gasson CE, Houston AI. Incorporating rules for responding into evolutionary games. Nature. 1999;401:368–371. PubMed

McNamara JM, Houston AI, Zoltán B, Osorno J-L. Should young ever be better off with one parent than with two? Nature. 2003;401:301–310.

Lack D. Courtship feeding in birds. Auk. 1940;57:169–178. doi: 10.2307/4078744. DOI

von Haartman L. The incubation rhythm of the female Pied Flycatcher (Ficedula hypoleuca) in the presence and absence of the male. Ornis Fenn. 1958;35:71–76.

Lyon BE, Montgomerie RD. Incubation feeding in snow buntings: female manipulation or indirect male parental care? Behav Ecol Sociobiol. 1985;17:279–284. doi: 10.1007/BF00300147. DOI

Chiver I, Morton ES, Stutchbury BJM. Incubation delays territory defence by male blue-headed vireos, Vireo solitarius. Anim Behav. 2007;73:143–148. doi: 10.1016/j.anbehav.2006.06.001. DOI

Williams TD. Physiological Adaptations for Breeding in Birds. Princeton and Oxford: Princeton University Press; 2012.

Schwagmeyer PL, Schwabl H, Mock D. Dynamics of biparental care in house sparrows: hormonal manipulations of paternal contributions. Anim Behav. 2005;69:481–488. doi: 10.1016/j.anbehav.2004.04.017. DOI

Smith LC, Raouf SA, Brown MB, Wingfield JC, Brown CR. Testosterone and group size in cliff swallows: testing the “challenge hypothesis” in a colonial bird. Horm Behav. 2005;47:76–82. doi: 10.1016/j.yhbeh.2004.08.012. PubMed DOI

Vleck CM. In: Avian Incubation: Behavior, Environment and Evolution. Deeming DC, editor. Oxford: Oxford University Press; 2002. Hormonal Control of Incubation Behaviour; pp. 54–62.

Magrath MJL, Komdeur J. Is male care compromised by additional mating opportunity? Trends Ecol Evol. 2003;18:424–430. doi: 10.1016/S0169-5347(03)00124-1. DOI

Stutchbury BJM, Morton ES. Behavioral Ecology of Tropical Birds. London: Academic Press; 2001.

Stutchbury BJM, Morton ES. Recent advances in the behavioral ecology of tropical birds. Wilson J Ornithol. 2008;120:26–37. doi: 10.1676/07-018.1. DOI

Cramer ERA, Hall ML, de Kort SR, Lovette IJ, Vehrencamp SL. Infrequent extra-pair paternity in the Banded Wren, a synchronously breeding tropical passerine. Condor. 2011;113:637–645. doi: 10.1525/cond.2011.100233. DOI

Macedo RH, Karubian J, Webster MS. Extrapair paternity and sexual selection in socially monogamous birds: are tropica birds different? Auk. 2008;125:769–777. doi: 10.1525/auk.2008.11008. DOI

Goymann W, Moore IT, Scheuerlein A, Hirschenhauser K, Grafen A, Wingfield JC. Testosterone in tropical birds: effects of environmental and social factors. Am Nat. 2004;164:327–334. doi: 10.1086/422856. PubMed DOI

Garamszegi LZ, Hirschenhauser K, V B, M E, S H-B, Møller AP, RF O, Wingfield JC. Latitudinal distribution, migration, and testosterone levels in birds. Am Nat. 2008;172:533–546. doi: 10.1086/590955. PubMed DOI

Eikenaar C, Husak J, Escallón C, Moore IT. Variation in testosterone and corticosterone in amphibians and reptiles: relationships with latitude, elevation, and breeding season length. Am Nat. 2012;180:642–654. doi: 10.1086/667891. PubMed DOI

De Heij ME, van der Graaf AJ, Hafner D, Tinbergen JM. Metabolic rate of nocturnal incubation in female great tits, Parus major, in relation to clutch size measured in a natural environment. J Exp Biol. 2007;210:2006–2012. doi: 10.1242/jeb.001420. PubMed DOI

Leisler B, Winkler H, Wink M. Evolution of breeding systems in acrocephaline warblers. Auk. 2002;119:379–390.

Wiersma P, Chappell M, Williams JB. Cold- and exercise-induced peak metabolic rates in tropical birds. Proc Natl Acad Sci USA. 2007;104:20866–20871. doi: 10.1073/pnas.0707683104. PubMed DOI PMC

Skutch AF. Life histories of Central American birds I. Families fringillidae, thraupidae, icteridae, parulidae and coerebidae. Pacific Coast Avifauna. 1954;31:1–448.

Skutch AF. Life histories of Central American birds II. Families vireonidae, sylviidae, turdidae, troglodytidae, paridae, corvidae, hirundinidae and tyrannidae. Pacific Coast Avifauna. 1960;34:1–593.

Skutch AF. Life histories of Central American birds III. Families cotingidae, pipridae, formicariidae, furnariidae, dendrocolaptidae, and picidae. Pacific Coast Avifauna. 1969;35:1–580.

Cramp S. The Birds of the Western Palearctic, Volume 5 Tyrant Flycatchers to Thrushes. Oxford: Oxford University Press; 1988.

Keith S, Urban EK, Fry HC. The Birds of Africa, Volume 4: Broadbills to Chats. London: Academic Press; 1992.

Poole A, Gill F. The Birds of North America. Philadelphia: The Birds of North America; 1992.

Cramp S, Brooks DJ. The Birds of the Western Palearctic, Volume 6. Oxford: Oxford University Press; 1992. (Warblers).

Cramp S, Perrins CM, Brooks DJ. The Birds of the Western Palearctic, Volume 7 Old World Flycatchers to Shrikes. Oxford: Oxford University Press; 1993.

Cramp S, Perrins CM. The Birds of the Western Palearctic, Volume 8 Crows to Finches. Oxford: Oxford University Press; 1994.

Urban EK, Fry HC, Keith S. The Birds of Africa, Volume V: Thrushes to Puffback Flycatchers. London: Academic Press; 1997.

Fry HC, Keith S, Urban EK. The Birds of Africa, Volume VI: Picathartes to Oxpeckers. London: Academic Press; 2000.

Higgins PJ, Peter JM. Handbook of Australian, New Zealand and Antarctic Birds. Vol. 6: Pardalotes to Shrike-Thrushes. Melbourne: Oxford University Press; 2002.

Higgins PJ, Peter JM, J CS. Handbook of Australian, New Zealand and Antarctic Birds. Vol. 7: Boatbill to Starlings. Melbourne: Oxford University Press; 2006.

Higgins PJ, Peter JM, Steele WK. Handbook of Australian, New Zealand and Antarctic Birds. Vol. 5: Tyrant-Flycatchers to Chats. Melbourne: Oxford University Press; 2001.

Ali S, Ripley DS. Handbook of the Birds of India and Pakistan. Together with Those of Bangladesh, Nepal, Sikkim, Bhutan and Sri Lanka (vol 1–10) 2. Dehli: Oxford University Press; 2002.

Fry HC, Keith S. The Birds of Africa, Volume VII: Sparrows to Buntings. London: Academic Press; 2004.

Hockey PAR, Dean WRJ, Ryan PG. Roberts Birds of Southern Africa. 7. Cape Town: Trustees of the John Voelcker Bird Book Fund; 2005.

Safford R, Hawkins F. The Birds of Africa, Volume VIII: The Malagasy Region. London: Christopher Helm; 2013.

Cramp S, Perrins CM. The Birds of the Western Palearctic, Volume 9 Buntings and New World Warblers. Oxford: Oxford University Press; 1994.

Skutch AF. The constancy of incubation. Wilson Bull. 1962;74:115–152.

Dunning JB. CRC Handbook of Avian Body Masses. 2. Boca Raton, Florida: CRC Press;

Del Hoyo J, Elliott JA, Christie DA. Handbook of the Birds of the World. Bush-Shrikes to Old World Sparrows. Barcelona: Lynx Edicions; 2009.

Harvey PH, Pagel MD. The Comparative Method in Evolutionary Biology. New York: Oxford University Press; 1991.

R Development Core Team. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2011.

Freckleton RP, Harvey PH, Pagel M. Phylogenetic analysis and comparative data: a test and review of evidence. Am Nat. 2002;160:712–726. doi: 10.1086/343873. PubMed DOI

Paradis E. Analysis of Phylogenetics and Evolution with R. 2. New York: Springer; 2012.

Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO. The global diversity of birds in space and time. Nature. 2012;491:444–448. doi: 10.1038/nature11631. PubMed DOI

Revell LJ. phytools: An R package for phylogenetic comparative biology (and other things) Methods Ecol Evol. 2012;3:217–223. doi: 10.1111/j.2041-210X.2011.00169.x. DOI

Anderson D. Model Based Inference in the Life Sciences: A Primer on Evidence. New York: Springer; 2007.

Rosenthal R. In: The Handbook of Research Synthesis. Cooper H, Hedges V, editor. New York: Russel Sage Foundation; 1994. Parametric Measures of Effect Size; pp. 231–244.

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