Hygric Niches for Tropical Endotherms
Authors: W. Alice Boyle, Elsie H. Shogren, Jeffrey D. Brawn
Journal: Trends in Ecology & Evolution (2020)

Precipitation regimes define patterns of tropical biogeography and seasonality, and are a strong selective force on tropical taxa.The mechanistic links between anomalies in rainfall and endotherm responses are poorly known, in contrast to an extensive literature on thermal physiology.Mounting evidence documents both positive and negative behavioral, physiological, and demographic responses to temporal variation in precipitation in birds and mammals.Anthropogenic changes in precipitation are spatially heterogeneous, involving increases or decreases in total rainfall combined with shifts in the timing and magnitude of rainfall events with unknown consequences for the majority of affected taxa.We fill a conceptual gap to expand the dimensionality of climatic niches required to interpret and predict precipitation responses based on organismal processes and thermal niche theory. Biotic selective pressures dominate explanations for the evolutionary ecology of tropical endotherms. Yet, abiotic factors, principally precipitation regimes, shape biogeographical and phenological patterns in tropical regions. Despite its importance, we lack a framework for understanding when, why, and how rain affects endotherms. Here, we review how tropical birds and mammals respond to rain at individual, population, and community levels, and propose a conceptual framework to interpret divergent responses. Diverse direct and indirect mechanisms underlie responses to rainfall, including physiological, top-down, and food-related drivers. Our framework constitutes a roadmap for the empirical studies required to understand the consequences of rainfall variability. Identifying the patterns and mechanisms underpinning responses to temporal variation in precipitation is crucial to anticipate consequences of anthropogenic climate change. Biotic selective pressures dominate explanations for the evolutionary ecology of tropical endotherms. Yet, abiotic factors, principally precipitation regimes, shape biogeographical and phenological patterns in tropical regions. Despite its importance, we lack a framework for understanding when, why, and how rain affects endotherms. Here, we review how tropical birds and mammals respond to rain at individual, population, and community levels, and propose a conceptual framework to interpret divergent responses. Diverse direct and indirect mechanisms underlie responses to rainfall, including physiological, top-down, and food-related drivers. Our framework constitutes a roadmap for the empirical studies required to understand the consequences of rainfall variability. Identifying the patterns and mechanisms underpinning responses to temporal variation in precipitation is crucial to anticipate consequences of anthropogenic climate change. Precipitation and temperature are the two major axes of global climatic variation. Whereas the paramount importance of precipitation regimes in plant biology is axiomatic [1.Boyce C.K. Lee J.-E. Plant evolution and climate over geological timescales.Annu. Rev. Earth Planet. Sci. 2017; 45: 61-87Crossref Scopus (26) Google Scholar], studies associating climate with animal evolutionary ecology and conservation have focused on thermal tolerances (see Glossary) (e.g., [2.Baudier K.M. et al.Extreme insolation: climatic variation shapes the evolution of thermal tolerance at multiple scales.Am. Nat. 2018; 192: 347-359Crossref PubMed Scopus (16) Google Scholar,3.Nadeau C.P. et al.Coarse climate change projections for species living in a fine-scaled world.Glob. Chang. Biol. 2017; 23: 12-24Crossref PubMed Scopus (0) Google Scholar]), owing to clear links between temperature and individual animal performance. In endotherms, as ambient temperatures deviate from thermal neutral zones, individuals compensate by actively generating or dissipating body heat; those responses are mediated by species- and individual-level traits [4.McKechnie A.E. Wolf B.O. The physiology of heat tolerance in small endotherms.Physiology. 2019; 34: 302-313Crossref PubMed Scopus (5) Google Scholar]. By contrast, we have a poor understanding of the mechanistic links between rainfall and the biology of terrestrial endotherms. This gap in knowledge has major implications for our ability to interpret macroecological patterns and predict climate change impacts [5.Bonebrake T.C. Mastrandrea M.D. Tolerance adaptation and precipitation changes complicate latitudinal patterns of climate change impacts.Proc. Natl. Acad. Sci. U. S. A. 2010; 107: 12581-12586Crossref PubMed Scopus (0) Google Scholar]. Precipitation is clearly critical to endotherm evolutionary ecology; for example, in species distribution models, the magnitude of modeled precipitation effects sometimes equals or exceeds that of temperature effects in both temperate and tropical environments (e.g., [6.Olson L.E. et al.Modeling the effects of dispersal and patch size on predicted Fisher (Pekania [Martes] pennanti) distribution in the US Rocky Mountains.Biol. Conserv. 2014; 169: 89-98Crossref Scopus (17) Google Scholar,7.MacPherson M.P. et al.Follow the rain? Environmental drivers of Tyrannus migration across the New World.Auk. 2018; 135: 881-894Crossref Scopus (4) Google Scholar]). However, associations between precipitation and distribution represent a black box in endotherm biology. Long- and short-term fluctuations in rainfall can affect terrestrial endotherms in multiple, but largely unstudied, ways. Furthermore, rainfall regimes are changing due to anthropogenic global change (Box 1). Without understanding the basis for relationships between precipitation and fitness, we cannot predict how changing precipitation will affect tropical endotherms in future decades. Although the concepts we present here apply to endotherms living in other environments, we focus on tropical forests and other tropical terrestrial communities, because identifying responses to variation in precipitation is more tractable in tropical systems, where there is less temperature seasonality than in temperate systems. Precipitation regimes define major plant associations, biogeographic provinces, and seasonality over most tropical regions [8.Holdridge L.R. Life Zone Ecology. Tropical Science Center, 1967Google Scholar,9.Vetaas O.R. et al.Principal factors controlling biodiversity along an elevation gradient: water, energy and their interaction.J. Biogeogr. 2019; 46: 1652-1663Crossref Scopus (8) Google Scholar]. Distributions of terrestrial animals closely match those of plant communities, and are likely shaped by combinations of direct, physiological responses to rainfall (analogous to thermal tolerances) and indirect responses mediated by species interactions [10.Barton M.G. et al.Incorporating temperature and precipitation extremes into process-based models of African Lepidoptera changes the predicted distribution under climate change.Ecol. Model. 2019; 394: 53-65Crossref Scopus (3) Google Scholar,11.Ficetola G.F. Maiorano L. Contrasting effects of temperature and precipitation change on amphibian phenology, abundance and performance.Oecologia. 2016; 181: 683-693Crossref PubMed Scopus (29) Google Scholar]. Food availability is the most-commonly invoked mediator of indirect responses (e.g., [12.De Carvalho W.D. et al.Reproductive constraints in frugivorous phyllostomid bats: seasonal and elevational variation in reproductive rates in the Brazilian Atlantic Forest.J. 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Tropical dry forest diversity, climatic response, and resilience in a changing climate.Forests. 2019; 10: 443Crossref Scopus (8) Google Scholar]. Particularly in arid tropical regions, food abundance clearly underlies demographic responses to interannual variation in rainfall, as seen, for example, in African savanna ungulate populations [16.Gandiwa E. et al.Rainfall variability and its impact on large mammal populations in a complex of semi-arid African savanna protected areas.Trop. Ecol. 2016; 57: 163-180Google Scholar]. Yet even in far wetter tropical regions, precipitation is still paramount in shaping biotic seasonality for producers and endotherm consumers [17.Reich P.B. Phenology of tropical forests: patterns, causes, and consequences. Can. J. Bot./Rev.Can. Bot. 1995; 73: 164-174Crossref Google Scholar, 18.Stouffer P.C. et al.Breeding seasonality in central Amazonian rainforest birds.Auk. 2013; 130: 529-540Crossref Scopus (39) Google Scholar, 19.van Schaik C.P. Brockman D.K. Seasonality in primate ecology, reproduction, and life history: an overview.in: Brockman D.K. van Schaik C.P. Seasonality in Primates: Studies of Living and Extinct Human and Non-Human Primates. Cambridge University Press, 2005: 3-20Crossref Google Scholar]. Ongoing phenological changes in the tropics are more strongly linked to changing precipitation regimes than to rising temperatures [20.Cohen J.M. et al.A global synthesis of animal phenological responses to climate change.Nat. Clim. Chang. 2018; 8: 224-228Crossref Scopus (86) Google Scholar]. Tropical regions are also subject to cyclical interannual variation in rainfall driven by the El Niño Southern Oscillation (ENSO), which manifests as changes in daily rainfall amounts, severity of storms, and duration of dry and wet seasons. Furthermore, endotherm physiology and energetics are affected by changes in humidity associated with precipitation [21.van Dyk M. et al.Interactions between humidity and evaporative heat dissipation in a passerine bird.J. Comp. Physiol. B Biochem. Syst. Environ. Physiol. 2019; 189: 299-308Crossref PubMed Scopus (5) Google Scholar]. Although tropical animals are clearly sensitive to both spatial and temporal variation in rainfall, the reasons for their responses are largely unknown [22.Sheldon K.S. Climate change in the tropics: ecological and evolutionary responses at low latitudes.Annu. Rev. Ecol. Evol. Syst. 2019; 50: 303-333Crossref Scopus (3) Google Scholar]. Here, we articulate a framework for understanding how, when, and why rain affects endothermic animals. The foundation of this framework is the concept of the 'hygric niche'. As with thermal niches, different mechanisms likely underlie relationships between performance and deviations from average conditions at opposite ends of the distributional limits of a species. However, mechanisms underlying hygric niches are diverse and not driven by physiological traits to the same extent as are thermal niches. Rather, they comprise multiple physiological, behavioral, and ecological processes, and myriad interspecific interactions (Table 1). We suggest that identifying underlying drivers is crucial to reconciling evidence of apparently individualistic functional relationships between rain and individual- or population-level performance, and for understanding and predicting responses to changing climates.Table 1Studies Exemplifying the Diversity of Endotherm Responses to Temporal Variation in PrecipitationTaxaStudy regionResponse variableNature of response (standardized relative to positive deviations in rainfall)Precipitation metricRefsIndividual-level responsesLance-tailed manakin (Chiroxiphia lanceolata)PanamaNestling growth ratePositiveSouthern Oceanic Niño Index (SOI)[101.Jones B.C. DuVal E.H. Direct and indirect effects of the El Niño Southern Oscillation on development and survival of young of a tropical passerine.Oecologia. 2019; 190: 485-496Crossref PubMed Scopus (1) Google Scholar]American redstart (Setophaga ruticilla)JamaicaSize-corrected body massPositiveDry season rainfall[111.Studds C.E. Marra P.P. Linking fluctuations in rainfall to nonbreeding season performance in a long-distance migratory bird, Setophaga ruticilla.Clim. Res. 2007; 35: 115-122Crossref Scopus (110) Google Scholar]Galápagos mockingbird (Mimus parvulus)Galápagos IslandsResponse to parasitism: nestling condition, parental provisioningPositiveBreeding season and annual rainfall[112.McNew S.M. et al.Annual environmental variation influences host tolerance to parasites.Proc. R. Soc. Lond. Ser. B: Biol. Sci. 2019; 28620190049PubMed Google Scholar]Sowell's short-tailed bat (Carollia sowelli)Costa RicaMetabolic rateNegativeWet (vs dry) experimental manipulation[57.Voigt C.C. et al.Rain increases the energy cost of bat flight.Biol. Lett. 2011; 7: 793-795Crossref PubMed Scopus (48) Google Scholar]Silvery mole-rat (Heliophobius argenteocinereus)MalawiDaily energy expenditureNegativeOnset of heavy rains[106.Zelová J. et al.A seasonal difference of daily energy expenditure in a free-living subterranean rodent, the Silvery Mole-Rat (Heliophobius argenteocinereus; Bathyergidae).Comp. Biochem. Physiol. A Mol. Integr. Physiol. 2011; 158: 17-21Crossref PubMed Scopus (13) Google Scholar]Population-level responsesPurple-crowned fairy-wren (Malurus coronatus coronatus)Northern AustraliaClutch sizePositiveRainfall 3 weeks before egg-laying[42.Hidalgo-Aranzamendi N. et al.Rapid plastic breeding response to rain matches peak prey abundance in a tropical savanna bird.J. Anim. Ecol. 2019; 88: 1799-1811Crossref PubMed Scopus (5) Google Scholar]Six species of cave-roosting insectivorous batsMalaysiaReproductive phenology: proportion of females lactatingPositiveRainfall in previous month[113.Nurul-Ain E. et al.Resource availability and roosting ecology shape reproductive phenology of rain forest insectivorous bats.Biotropica. 2017; 49: 382-394Crossref Scopus (9) Google Scholar]Verreaux's sifaka (Propithecus verreauxi)MadagascarInfant survival, fertility ratesPositiveMonthly rainfall, Indian Ocean Dipole (IOD)[25.Campos F.A. et al.Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species.Global Change Biol. 2017; 23: 4907-4921Crossref PubMed Scopus (14) Google Scholar]Milne Edward's sifaka (Propithecus edwardsi)MadagascarFecundityNegativeENSO[26.Dunham A.E. et al.Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar.Glob. Chang. Biol. 2011; 17: 219-227Crossref Scopus (63) Google Scholar]Wire-tailed manakin (Pipra filicauda)EcuadorSurvival, condition, recruitment, lek sizeNegativeENSO phase (lower survival and condition following La Niña years)[102.Ryder T.B. Sillett T.S. Climate, demography and lek stability in an Amazonian bird.Proc. R. Soc. Lond. Ser. B Biol. Sci. 2016; 28320152314Crossref PubMed Scopus (13) Google Scholar]Lowland moist forest birdsPanamaPopulation growth rates of multiple speciesMixed responses; more negative than positiveDry season length[67.Brawn J.D. et al.Impacts of changing rainfall regime on the demography of tropical birds.Nat. Clim. Chang. 2017; 7: 133-136Crossref Scopus (17) Google Scholar]Community-level responsesMid-elevation arid forest mammalsIndiaAbundancePositiveENSO[114.Waite T.A. et al.La Niña's signature: synchronous decline of the mammal community in a 'protected' area in India.Divers. Distrib. 2007; 13: 752-760Crossref Scopus (0) Google Scholar]Lowland wet forest terrestrial mammalsPeruDensity of individualsNegativeFlooding, measured as meters above sea level[50.Bodmer R. et al.Major shifts in Amazon wildlife populations from recent intensification of floods and drought.Conserv. Biol. 2018; 32: 333-344Crossref PubMed Scopus (9) Google Scholar]Trophic cascades involving wildebeest (Connochaetes taurinus)aThis paper evaluated the consequences of rainfall on three sets of trophic relationships. We highlight here interactions involving wildebeest, but in all cases where relationships were statistically significant, rain was positively associated with density, foraging rates, recruitment, and other demographic parameters.SerengetiWildebeest recruitment; lion prey intakePositiveSOI[39.Sinclair A.R.E. et al.Asynchronous food-web pathways could buffer the response of Serengeti predators to El Niño Southern Oscillation.Ecology. 2013; 94: 1123-1130Crossref PubMed Scopus (0) Google Scholar]Lowland wet forest birdsEcuadorAbundance: estimated from captures and observationsNegativeSOI, dry-season rainfall[115.Blake J.G. Loiselle B.A. Enigmatic declines in bird numbers in lowland forest of eastern Ecuador may be a consequence of climate change.PeerJ. 2015; 3e1177Crossref PubMed Scopus (18) Google Scholar]Lowland dry forest small mammalsMexicoSpecies richnessPositiveRainfall during previous wet season[116.Mason-Romo E.D. et al.Two decades of climate driving the dynamics of functional and taxonomic diversity of a tropical small mammal community in western Mexico.PLoS ONE. 2017; 12e0189104Crossref PubMed Scopus (3) Google Scholar]a This paper evaluated the consequences of rainfall on three sets of trophic relationships. We highlight here interactions involving wildebeest, but in all cases where relationships were statistically significant, rain was positively associated with density, foraging rates, recruitment, and other demographic parameters. Open table in a new tab How do endotherms fare when conditions are drier or wetter than average? The evidence is mixed; wetter years are often 'good' years for some endotherms, whereas, for others, survival or fecundity increases in drier-than-average years [23.Woodworth B.K. et al.Hot temperatures during the dry season reduce survival of a resident tropical bird.Proc. R. Soc. Lond., Ser. B: Biol. Sci. 2018; 28520180176PubMed Google Scholar, 24.Santillan V. et al.Spatio-temporal variation in bird assemblages is associated with fluctuations in temperature and precipitation along a tropical elevational gradient.PLoS ONE. 2018; 13e0196179Crossref PubMed Scopus (6) Google Scholar, 25.Campos F.A. et al.Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species.Global Change Biol. 2017; 23: 4907-4921Crossref PubMed Scopus (14) Google Scholar, 26.Dunham A.E. et al.Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar.Glob. Chang. Biol. 2011; 17: 219-227Crossref Scopus (63) Google Scholar]. Moreover, populations of a single species can respond differently to variation in rainfall across their range [27.Grosbois V. et al.Climate impacts on Mediterranean blue tit survival: an investigation across seasons and spatial scales.Glob. Chang. Biol. 2006; 12: 2235-2249Crossref Scopus (38) Google Scholar] (Table 1); indeed, 70 years ago, Skutch documented differences in phenology of yellow-faced grassquits (Tiaris olivaceus) associated with rainfall regime, with reproduction starting during the dry season in wet areas, and during the wet season in dry areas [28.Skutch A.F. The nesting seasons of Central American birds in relation to climate and food supply.Ibis. 1950; 92: 185-222Crossref Scopus (76) Google Scholar]. We propose a hygric niche concept in hope of reconciling divergent responses to temporal variation in rainfall among populations, and among species within the same community (Figure 1). We follow Chase and Leibold ([29.Chase J.M. Leibold M.A. Ecological Niches. University of Chicago Press, 2003Crossref Google Scholar] p. 19) in defining a species' niche as 'the environmental conditions that allow a species to satisfy its minimum requirements so that the birth rate of a local population is equal to or greater than its death rate along with the set of per capita impacts of that species on these environmental conditions' and follow in the footsteps of Whittaker [30.Whittaker R.H. Gradient analysis of vegetation.Biol. Rev. 1967; 42: 207-264Crossref PubMed Google Scholar] in the graphical depiction of niches along environmental gradients. We adopt a mechanistic approach to describing ecological hygric niches, amenable to testing using experimental and statistical distributional approaches [31.Holt R.D. Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives.Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 19659-19665Crossref PubMed Scopus (377) Google Scholar]. A core assumption of the hygric niche model is that endotherms exhibit curvilinear performance responses along precipitation gradients, just as they do along temperature gradients [32.Angilletta M.J. Thermal Adaptation: A Theoretical and Empirical Synthesis. Oxford University Press, 2009Crossref Google Scholar]. Thus, performance should peak near the center of the precipitation conditions that the species tolerates, and performance should decline toward wetter and drier extremes (Figure 1A). Precipitation–performance curves may be roughly Gaussian, asymmetric, or exhibit thresholds or neutral responses over portions of the gradient. The aggregate of individual performances contributes to shaping population-level demographic responses to interannual variation in rainfall (subject to several assumptions [33.Sinclair B.J. et al.Can we predict ectotherm responses to climate change using thermal performance curves and body temperatures?.Ecol. Lett. 2016; 19: 1372-1385Crossref PubMed Scopus (206) Google Scholar]). In our model, we depict the niches of species (Figure 1B) to be narrower than individual hygric tolerances in part because the conditions required for successful reproduction are more stringent than those under which an individual can potentially survive [34.Gvoždík L. Just what is the thermal niche?.Oikos. 2018; 127: 1701-1710Crossref Scopus (8) Google Scholar]. Species and individual curves also differ in shape or breadth due to the differences between requirements for populations to persist (allowing for demographic rescue via dispersal) and conditions required for populations to thrive (i.e., persistence vs. establishment niches [31.Holt R.D. Bringing the Hutchinsonian niche into the 21st century: ecological and evolutionary perspectives.Proc. Natl. Acad. Sci. U. S. A. 2009; 106: 19659-19665Crossref PubMed Scopus (377) Google Scholar]). Conversely, local adaptation could lead to flatter and broader species-specific hygric response curves relative to individual performance curves. Regardless of their shape and breadth, near the middle of species-level hygric niches, we expect populations to exhibit weak or inconsistent responses to temporal deviations in rainfall because neither modest increases nor decreases in rain will result in conditions approaching the extremes tolerated by that species (Figure 1B). However, populations living near dry extremes of the niche should respond strongly and positively to wetter-than-average conditions, because wet years will approximate environments closer to species-specific optima. Those same populations should respond negatively to drier-than-average conditions, because droughts years will approximate environments located at or beyond those in which individuals can survive and reproduce. Populations near the wet extreme of the niche will exhibit opposite responses to temporal variation in rainfall. The important axes of interannual variation in rainfall may manifest as overall precipitation totals, the timing and duration of rainy and dry seasons, and/or the intensity of wet and dry periods. Just as each species exhibits unique demographic responses to thermal gradients, we expect them also to exhibit species-specific responses to precipitation regimes (Figure 1C). Many direct (physiological) and indirect (biotically mediated) mechanisms underlie rainfall–demographic relationships. Even within species, different mechanisms may link precipitation to survival or reproduction at opposite ends of the hygric niche. The idea that bottom-up processes, specifically food availability, drives endotherm population dynamics pervades most interpretations of individual, population-level, or distributional responses to precipitation in tropical communities (e.g., [35.Sluydts V. et al.Survival and maturation rates of the African rodent, Mastomys natalensis: density-dependence and rainfall.Integr. Zool. 2007; 2: 220-232Crossref PubMed Google Scholar]). At low elevations in the tropics, plant productivity is often constrained by soil moisture [36.Seiler C. et al.The sensitivity of wet and dry tropical forests to climate change in Bolivia.J. Geophys. Res. Biogeosci. 2015; 120: 399-413Crossref Scopus (11) Google Scholar]; locations having pronounced dry seasons experience deficits in soil moisture for periods of days to months, reducing primary productivity [37.Zimmerman J.K. et al.Flowering and fruiting phenologies of seasonal and aseasonal Neotropical forests: the role of annual changes in irradiance.J. Trop. Ecol. 2007; 23: 231-251Crossref Scopus (112) Google Scholar]. Thus, in a wetter-than-average year, the severity and duration of moisture deficits will typically decline [9.Vetaas O.R. et al.Principal factors controlling biodiversity along an elevation gradient: water, energy and their interaction.J. Biogeogr. 2019; 46: 1652-1663Crossref Scopus (8) Google Scholar], leading to increasing primary productivity; the reverse will occur in dry years [38.Vilanova E. et al.Environmental drivers of forest structure and stem turnover across Venezuelan tropical forests.PLoS ONE. 2018; 13e0198489Crossref PubMed Scopus (4) Google Scholar]. Such bottom-up processes are fundamental to structuring endotherm communities in tropical grassland systems (most notably in the Serengeti [39.Sinclair A.R.E. et al.Asynchronous food-web pathways could buffer the response of Serengeti predators to El Niño Southern Oscillation.Ecology. 2013; 94: 1123-1130Crossref PubMed Scopus (0) Google Scholar]). In forests, interannual variation in precipitation affects leaf production and flower, fruit, and seed production, which in turn affects food availability at higher trophic levels [40.Butt N. et al.Cascading effects of climate extremes on vertebrate fauna through changes to low-latitude tree flowering and fruiting phenology.Glob. Chang. Biol. 2015; 21: 3267-3277Crossref PubMed Scopus (0) Google Scholar]. Elevated food availability affects endotherm foraging efficiency, which can influence reproductive investment and survival at all life stages. Such cascading implications of rainfall-mediated fluctuations in food and competition underlie well-known examples of trait evolution in Darwin's finches [41.Grant P.R. Grant B.R. Evolution of character displacement in Darwin's finches.Science. 2006; 313: 224-226Crossref PubMed Scopus (524) Google Scholar] and drive rapid, plastic reproductive responses to the onset of rains in tropical grasslands and savannas (e.g., [42.Hidalgo-Aranzamendi N. et al.Rapid plastic breeding response to rain matches peak prey abundance in a tropical savanna bird.J. Anim. Ecol. 2019; 88: 1799-1811Crossref PubMed Scopus (5) Google Scholar]). The assumption that food-driven, bottom-up mechanisms lead to positive responses in wetter years and negative responses in drier years is not universally true. For example, in Panama, plants produce synchronous crops of higher-quality leaves and increase energy allocation to flowers and fruits in dry years with less rain and more sunlight. The increase in leaf nutrients and reproductive structures results in more arthropod prey for endotherm consumers [43.Van Bael S.A. Brawn J.D. The direct and indirect effects of insectivory by birds in two contrasting Neotropical forests.Oecologia. 2005; 143: 106-116Crossref PubMed Scopus (0) Google Scholar,44.Wright S.J. Calderón O. Seasonal, El Niño and longer term changes in flower and seed production in a moist tropical forest.Ecol. Lett. 2006; 9: 35-44PubMed Google Scholar]. Furthermore, factors other than food availability may regulate populations. For example, changes in predation pressure and parental vigilance may underlie associations between precipitation and fledging success of understory tropical birds [45.Tarwater C.E. et al.Parental response to elevated begging in a high predation, tropical environment.Anim. Behav. 2009; 78: 1239-1245Crossref Scopus (18) Google Scholar]. Therefore, rainfall-driven demographic or behavioral changes in predator communities could influence fecundity more strongly than could bottom-up processes. Finally, direct risks of dehydration under arid conditions can influence the behavior of tropical primates [46.Sato H. Predictions of seed shadows generated by common brown lemurs (Eulemur fulvus) and their relationship to seasonal behavioral strategies.Int. J. Primatol. 2018; 39: 377-396Crossref Scopus (2) Google Scholar] and birds [47.Molokwu M.N. et al.Effects of season, water and predation risk on patch use by birds on the African savannah.Oecologia. 2010; 164: 637-645Crossref PubMed Scopus (15) Google Scholar], indicating the potential for physiologically mediated direct responses to rain. Thus, even at the dry end of the hygric niche of a species, it is not safe to assume that food-driven processes underlie all positive associations between demography and rainfall. Negative relationships between rain and fitness at the wet ends of hygric niches are less intuitive and likely involve a broad suite of direct and indirect mechanisms. Direct consequences of rain include mortality during storms due to elevated energetic cost