Abstract:

Climate change will likely be the most significant challenge faced by species in this century, and species’ ability to cope with climate change depends on their life history and ecological and evolutionary traits. Understanding how these traits mediate species’ responses is beneficial for identifying more vulnerable species or prone to extinction risk. Here, we carried out a literature review describing how four traits commonly used in vulnerability assessments (i.e. clutch size, diet breadth, dispersal ability, and climatic tolerance) may determine species vulnerability. We also portray the possible mechanisms that explain how these traits govern species responses to climate change. The literature suggests different mechanisms operating for the evaluated traits. The mechanism of response to climate change differs between species inhabiting tropical and temperate regions: while species from the temperate areas may respond positively to temperature rise, tropical species may be severely affected. Since ectotherms depend on environment temperature, they are more sensitive and present different response mechanisms from endotherms.

Keywords:
Global warming; extinction risk; phenology; physiology; species traits

Resumo:

A mudança climática provavelmente será o maior desafio enfrentado pelas espécies neste século e a capacidade das espécies em lidar com a mudança climática depende de seus próprios atributos de história de vida, ecológicos e evolutivos. Entender como esses atributos mediam as respostas das espécies é extremamente útil para identificar espécies que são mais vulneráveis ou sujeitas ao risco de extinção. Aqui, realizamos uma revisão da literatura com foco na descrição de como quatro atributos comumente usados em avaliações de vulnerabilidade (tamanho da ninhada, amplitude da dieta, capacidade de dispersão e tolerância climática) podem realmente determinar a vulnerabilidade das espécies. Também retratamos os possíveis mecanismos que explicam como esses atributos governam as respostas das espécies à mudança climática. A literatura sugere diferentes mecanismos operando para os atributos avaliados. O mecanismo de resposta à mudança climática difere entre as espécies que habitam as regiões tropicais e temperadas: enquanto as espécies das regiões temperadas podem responder positivamente ao aumento da temperatura, as espécies tropicais podem ser severamente afetadas. Como os ectotérmicos dependem da temperatura ambiente, eles são mais sensíveis e apresentam mecanismos de resposta diferentes dos endotérmicos.

Palavras-chave:
Aquecimento global; risco de extinção; fenologia; fisiologia; atributos das espécies

Introduction

Climate change will likely be the most significant challenge faced by species this century. The observed effects include changes in distribution areas, phenology, morphology, demography, and abundance (Parmesan and Yohe 2003Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42. doi: 10.1038/nature01286
https://doi.org/10.1038/nature01286... ; Parmesan 2006Parmesan C (2006) Ecological and Evolutionary Responses to Recent Climate Change. Annual Review of Ecology, Evolution, and Systematics 37:637-669. doi: 10.1146/annurev.ecolsys.37.091305.110100
https://doi.org/10.1146/annurev.ecolsys.... ; Lane et al. 2012Lane JE, Kruuk LEB, Charmantier A, et al (2012) Delayed phenology and reduced fitness associated with climate change in a wild hibernator. Nature 489:554-557. doi: 10.1038/nature11335
https://doi.org/10.1038/nature11335... ). Species ability to respond to climate change depends on their life-history traits (Végvári et al. 2010Végvári Z, Bókony V, Barta Z, Kovács G (2010) Life history predicts advancement of avian spring migration in response to climate change. Global Change Biology 16:1-11. doi: 10.1111/j.1365-2486.2009.01876.x
https://doi.org/10.1111/j.1365-2486.2009... ; Angert et al. 2011Angert AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecology Letters 14:677-689. doi: 10.1111/j.1461-0248.2011.01620.x
https://doi.org/10.1111/j.1461-0248.2011... ; Pacifici et al. 2017Pacifici M, Visconti P, Butchart SHM, et al (2017) Species’ traits influenced their response to recent climate change. Nature Climate Change 7:205-208. doi: 10.1038/nclimate3223
https://doi.org/10.1038/nclimate3223... ), which can help predict species that will be more vulnerable and direct conservation efforts (Foden et al. 2013Foden WB, Butchart SHM, Stuart SN, et al (2013) Identifying the World’s Most Climate Change Vulnerable Species: A Systematic Trait-Based Assessment of all Birds, Amphibians and Corals. PLoS ONE 8:. doi: 10.1371/journal.pone.0065427
https://doi.org/10.1371/journal.pone.006... ).

In this sense, the use of trait-based Climate Change Vulnerability Assessments (CCVAs) has become popular in studies that assess climate change impact on species vulnerability (Foden et al. 2018Foden WB, Young BE, Akçakaya HR, et al (2018) Climate change vulnerability assessment of species. Wiley Interdisciplinary Reviews: Climate Change e551. doi: 10.1002/wcc.551
https://doi.org/10.1002/wcc.551... ). In the context of CCVAs, the term “trait” refers to a wide range of species characteristics (such as diet breadth and climatic tolerance) instead of referring to specific features of an individual (sensu Violle et al. 2007Violle C, Navas M, Vile D, et al (2007) Let the concept of trait be functional! Oikos 882-892. doi: 10.1111/j.2007.0030-1299.15559.x
https://doi.org/10.1111/j.2007.0030-1299... ). Trait-based CCVAs combine scores based on exposure to climate change (extrinsic factors) with biological characteristics of species (intrinsic factors), which define their sensitivity and adaptive capacity to obtain a general measure of vulnerability (Pacifici et al. 2015Pacifici M, Foden WB, Visconti P, et al (2015) Assessing species vulnerability to climate change. Nature Climate Change 5:215-225. doi: 10.1038/nclimate2448
https://doi.org/10.1038/nclimate2448... ).

Vulnerability is assessed based on these three components: exposure, sensitivity, and adaptive capacity, so that species with high exposure, high sensitivity, and low adaptive capacity will be the most vulnerable to climate change (Dawson et al. 2011Dawson TP, Jackson ST, House JI, et al (2011) Beyond predictions: biodiversity conservation in a changing climate. Science (New York, NY) 332:53-58. doi: 10.1126/science.1200303
https://doi.org/10.1126/science.1200303... ; Foden et al. 2013Foden WB, Butchart SHM, Stuart SN, et al (2013) Identifying the World’s Most Climate Change Vulnerable Species: A Systematic Trait-Based Assessment of all Birds, Amphibians and Corals. PLoS ONE 8:. doi: 10.1371/journal.pone.0065427
https://doi.org/10.1371/journal.pone.006... ). Exposure is determined by the rate and magnitude of climate change within the species’ distribution area. Sensitivity is characterised by the ability to tolerate climate change and is generally associated with physiological tolerance and habitat specialisation. Adaptive capacity refers to the ability of a given species to deal with climate change, whether adapting to new local conditions or dispersing to more suitable areas (Dawson et al. 2011Dawson TP, Jackson ST, House JI, et al (2011) Beyond predictions: biodiversity conservation in a changing climate. Science (New York, NY) 332:53-58. doi: 10.1126/science.1200303
https://doi.org/10.1126/science.1200303... ).

Despite the importance of biological traits in determining species vulnerability, there is no agreement on which traits should be used in assessments. Their selection depends on data availability and the opinion of experts (Foden et al. 2013Foden WB, Butchart SHM, Stuart SN, et al (2013) Identifying the World’s Most Climate Change Vulnerable Species: A Systematic Trait-Based Assessment of all Birds, Amphibians and Corals. PLoS ONE 8:. doi: 10.1371/journal.pone.0065427
https://doi.org/10.1371/journal.pone.006... , 2018). Biological traits may help identify species with higher extinction risk (Mckinney 1997Mckinney ML (1997) EXTINCTION VULNERABILITY AND SELECTIVITY : Combining Ecological and Paleontological Views. 495-516; Purvis and Hector 2000Purvis A, Hector A (2000) Getting the measure of biodiversity. Nature 405:212-219). However, species responses depend on the type of threat they are exposed to (González-Suarez et al. 2013González-Suarez M, Gomez A, Revilla E (2013) Which intrinsic traits predict vulnerability to extinction depends on the actual threatening processes. Ecosphere 4:1-16). Species that present larger body size is more threatened by hunting, while smaller and ecologically specialised species are more threatened by habitat loss and fragmentation (Owens and Bennett 2000Owens IPF, Bennett PM (2000) Ecological basis of extinction risk in birds: Habitat loss versus human persecution and introduced predators. Proceedings of the National Academy of Sciences 97:12144-12148. doi: 10.1073/pnas.200223397
https://doi.org/10.1073/pnas.200223397... ; González-Suarez et al. 2013González-Suarez M, Gomez A, Revilla E (2013) Which intrinsic traits predict vulnerability to extinction depends on the actual threatening processes. Ecosphere 4:1-16).

Under the threat of climate change, biological traits might play a fundamental role in species responses, influencing their vulnerability (Jiguet et al. 2007Jiguet F, Gadot A-S, Julliard R, et al (2007) Climate envelope, life history traits and the resilience of birds facing global change. Global Change Biology 1672-1684. doi: 10.1111/j.1365-2486.2007.01386.x
https://doi.org/10.1111/j.1365-2486.2007... ; Angert et al. 2011Angert AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecology Letters 14:677-689. doi: 10.1111/j.1461-0248.2011.01620.x
https://doi.org/10.1111/j.1461-0248.2011... ; Estrada et al. 2015Estrada A, Meireles C, Morales-castilla I, et al (2015) Species’ intrinsic traits inform their range limitations and vulnerability under environmental change. Global Ecology and Biogeography 849-858. doi: 10.1111/geb.12306
https://doi.org/10.1111/geb.12306... ). Clutch size is strongly influenced by climatic variables (Jetz et al. 2008Jetz W, Sekercioglu CH, Bohning-Gaese K (2008) The Worldwide Variation in Avian Clutch Size across Species and Space. PLoS Biology 6:e303. doi: 10.1371/journal.pbio.0060303
https://doi.org/10.1371/journal.pbio.006... ), and species may present rapid physiological adjustments of this trait in response to climatic changes (Baker 1995Baker M (1995) Environmental Component of Latitudinal Clutch-Size Variation in House Sparrows (Passer domesticus). The Auk 112:249-252; Coe and Rotenberry 2003Coe SJ, Rotenberry JT (2003) WATER AVAILABILITY AFFECTS CLUTCH SIZE IN A DESERT SPARROW. Ecology 84:3240-3249). Species that reproduce frequently or prematurely, with high fecundity, should have greater opportunities to colonise new environments (Angert et al. 2011Angert AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecology Letters 14:677-689. doi: 10.1111/j.1461-0248.2011.01620.x
https://doi.org/10.1111/j.1461-0248.2011... ). Species with generalist diets can change their feeding habits to other resources when climate affects the availability of preferred items (Rubolini et al. 2003Rubolini D, Pirovano A, Borghi S (2003) Influence of seasonality, temperature and rainfall on the winter diet of the long-eared owl, Asio otus. Folia Zoologica 52:67-76; Bojarska and Selva 2012Bojarska K, Selva N (2012) Spatial patterns in brown bear Ursus arctos diet: the role of geographical and environmental factors. Mammal Review 42:120-143. doi: 10.1111/j.1365-2907.2011.00192.x
https://doi.org/10.1111/j.1365-2907.2011... ) and, consequently, they might have a higher ability to change their distributions to follow suitable climatic conditions (Angert et al. 2011Angert AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecology Letters 14:677-689. doi: 10.1111/j.1461-0248.2011.01620.x
https://doi.org/10.1111/j.1461-0248.2011... ). Dispersal ability is a crucial trait that allows species to change their distribution areas to follow a suitable climate. Species with higher dispersal ability might respond more quickly to climate change, facing lower extinction risk (Pöyry et al. 2009Pöyry J, Luoto M, Heikkinen R, et al (2009) Species traits explain recent range shifts of Finnish butterflies. Global Change Biology 15:732-743. doi: 10.1111/j.1365-2486.2008.01789.x
https://doi.org/10.1111/j.1365-2486.2008... ; Corlett and Westcott 2013Corlett RT, Westcott DA (2013) Will plant movements keep up with climate change? Trends in Ecology & Evolution 28:482-488. doi: 10.1016/j.tree.2013.04.003
https://doi.org/10.1016/j.tree.2013.04.0... ). Species that can physiologically tolerate higher climatic variation and live in environments where temperatures are far from their upper thermal limit will be more likely to persist under climate change (Deutsch et al. 2008Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... ; Huey et al. 2012Huey RB, Kearney MR, Krockenberger A, et al (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B: Biological Sciences 367:1665-1679. doi: 10.1098/rstb.2012.0005
https://doi.org/10.1098/rstb.2012.0005... ). There is a growing interest in using biological traits to assess species vulnerability in response to climate change (Gardali et al. 2012Gardali T, Seavy NE, Digaudio RT, Comrack LA (2012) A Climate Change Vulnerability Assessment of California’ s At-Risk Birds. PLoS ONE 7:. doi: 10.1371/journal.pone.0029507
https://doi.org/10.1371/journal.pone.002... ; Foden et al. 2013Foden WB, Butchart SHM, Stuart SN, et al (2013) Identifying the World’s Most Climate Change Vulnerable Species: A Systematic Trait-Based Assessment of all Birds, Amphibians and Corals. PLoS ONE 8:. doi: 10.1371/journal.pone.0065427
https://doi.org/10.1371/journal.pone.006... ; Garcia et al. 2014Garcia RA, Araújo MB, Burgess ND, et al (2014) Matching species traits to projected threats and opportunities from climate change. Journal of Biogeography 41:724-735. doi: 10.1111/jbi.12257
https://doi.org/10.1111/jbi.12257... ; Böhm et al. 2016Böhm M, Cook D, Ma H, et al (2016) Hot and bothered: Using trait-based approaches to assess climate change vulnerability in reptiles. Biological Conservation 204:32-41. doi: 10.1016/j.biocon.2016.06.002
https://doi.org/10.1016/j.biocon.2016.06... ; Reside et al. 2016Reside AE, Vanderwal J, Garnett ST, Kutt AS (2016) Vulnerability of Australian tropical savanna birds to climate change. Austral Ecology 41:106-116. doi: 10.1111/aec.12304
https://doi.org/10.1111/aec.12304... ; Borges et al. 2019Borges FJA, Ribeiro BR, Lopes LE, Loyola R (2019) Bird vulnerability to climate and land use changes in the Brazilian Cerrado. Biological Conservation 236:347-355. doi: 10.1016/j.biocon.2019.05.055
https://doi.org/10.1016/j.biocon.2019.05... ). However, potentially important traits from some taxa are still frequently unavailable, which leads to the use of morphological proxies, measurements from congeneric species or the knowledge of experts (Foden et al. 2013Foden WB, Butchart SHM, Stuart SN, et al (2013) Identifying the World’s Most Climate Change Vulnerable Species: A Systematic Trait-Based Assessment of all Birds, Amphibians and Corals. PLoS ONE 8:. doi: 10.1371/journal.pone.0065427
https://doi.org/10.1371/journal.pone.006... , 2018Foden WB, Young BE, Akçakaya HR, et al (2018) Climate change vulnerability assessment of species. Wiley Interdisciplinary Reviews: Climate Change e551. doi: 10.1002/wcc.551
https://doi.org/10.1002/wcc.551... ).

Identifying the most informative traits and responding to climate change is a priority if we want to assess the vulnerability of different species groups. However, a study showed that less than half of the studies that evaluated the relationship between traits and changes in species distributions have specified hypothesis for the ecological processes involved in the relationship (Estrada et al. 2016Estrada A, Morales-castilla I, Caplat P, Early R (2016) Usefulness of Species Traits in Predicting Range Shifts. Trends in Ecology & Evolution 31:190-203. doi: 10.1016/j.tree.2015.12.014
https://doi.org/10.1016/j.tree.2015.12.0... ). To advise appropriate conservation measures, it is essential to explain the reasons for choosing traits and the specific mechanisms underlying climate change impacts on species of interest (Foden et al. 2018Foden WB, Young BE, Akçakaya HR, et al (2018) Climate change vulnerability assessment of species. Wiley Interdisciplinary Reviews: Climate Change e551. doi: 10.1002/wcc.551
https://doi.org/10.1002/wcc.551... ).

We did a literature review to understand how four traits (clutch size, diet breadth, dispersal ability and climatic tolerance) might determine species vulnerability. We also aimed to describe the possible mechanisms that explain how traits influence species responses to climatic changes. Specifically, our goals were: 1) to verify whether it is possible to use the four chosen traits to understand the mechanisms underlying the impacts caused by climate change based on the ecology literature produced so far, and 2) to present and explain the main mechanisms found. Including details regarding these mechanisms will help substantiate trait choice and broaden the discussion about future conservation strategies of assessed species.

Material and Methods

We searched the literature for studies that evaluated variation in the four traits mentioned earlier in response to recent climate change regarding organisms from any taxa within any level (population, community, and ecosystem). We chose these four traits because they are commonly used in CCVAs (Gardali et al. 2012Gardali T, Seavy NE, Digaudio RT, Comrack LA (2012) A Climate Change Vulnerability Assessment of California’ s At-Risk Birds. PLoS ONE 7:. doi: 10.1371/journal.pone.0029507
https://doi.org/10.1371/journal.pone.002... ; Reside et al. 2016Reside AE, Vanderwal J, Garnett ST, Kutt AS (2016) Vulnerability of Australian tropical savanna birds to climate change. Austral Ecology 41:106-116. doi: 10.1111/aec.12304
https://doi.org/10.1111/aec.12304... ; Borges et al. 2019Borges FJA, Ribeiro BR, Lopes LE, Loyola R (2019) Bird vulnerability to climate and land use changes in the Brazilian Cerrado. Biological Conservation 236:347-355. doi: 10.1016/j.biocon.2019.05.055
https://doi.org/10.1016/j.biocon.2019.05... ) and are more widely available in the literature. As the study’s objective was to present a broad discussion for each trait, more traits would excessively increase the number of pages in the study. The search was carried out in July 2019 in the Thomson Reuters ISI Web of Science online database. It included articles published between 1945 and 2019, using the following search terms: (“trait” OR “clutch size” OR “diet” OR “dispersion” OR “climatic tolerance” OR “thermic tolerance” OR “heat tolerance”) AND (“climate change” OR “global warming” OR “temperature increase”).

We excluded studies that: (1) belonged to Web of Science categories not related to ecology (e.g. agronomy, veterinary medicine, tropical medicine), (2) did not relate (directly or indirectly) possible trait changes to climate change, and (3) did not present any explanation (through empirical data) to the mechanisms involved in the observed responses (e.g. changes in distribution areas, phenology and abundance). Studies cited by the articles obtained in our search were also included in our synthetic review if they fulfilled the requirements. The search generated a total of 1164 articles. After the exclusions following the criteria mentioned above, 197 articles were evaluated.

Results and Discussion

1. Clutch size

Clutch size is one of the best-studied life-history traits in birds, and its variation throughout the latitude gradient is well known, with larger clutch size in higher latitudes (Lack 1947Lack D (1947) The significance of clutch-size. Part I - Intraespecific variation. Ibis 89:302-352; Skutch 1949Skutch AF (1949) DO TROPICAL BIRDS REAR AS MANY YOUNG AS THEY CAN NOURISH? Ibis 91:430-455; Ashmole 1963Ashmole NP (1963) The regulation of numbers of tropical oceanic birds. Ibis 103b:458-473 ; Ricklefs 1980Ricklefs RE (1980) Geographical Variation in Clutch Size among Passerine Birds: Ashmole’s Hypothesis. The Auk 97:38-49; Evans et al. 2005Evans KL, Duncan RP, Blackburn TM, Crick HQP (2005) Investigating geographic variation in clutch size using a natural experiment. Functional Ecology 19:616-624. doi: 10.1111/j.1365-2435.2005.01016.x
https://doi.org/10.1111/j.1365-2435.2005... ; Jetz et al. 2008Jetz W, Sekercioglu CH, Bohning-Gaese K (2008) The Worldwide Variation in Avian Clutch Size across Species and Space. PLoS Biology 6:e303. doi: 10.1371/journal.pbio.0060303
https://doi.org/10.1371/journal.pbio.006... ). As expected, studies that assess clutch size are focused on birds and have been carried out mainly in the temperate region (Table 1). Birds that inhabit temperate and tropical areas adopt different life-history strategies to respond to climate change through other mechanisms (Table 1).

Clutch size is related to species fecundity; thus, it indicates the population ability to recruit. Species with smaller clutch size present low reproductive potential and consequently a slower response to risk factors, which would make them more vulnerable to decline and extinction (Smith and Quin 1996Smith AP, Quin DG (1996) PATTERNS AND CAUSES OF EXTINCTION AND DECLINE IN AUSTRALIAN CONILURINE RODENTS. Biological Conservation 3207:243-267; Pimm 1991Pimm SL (1991) The balance of nature? Chicago: University of Chicago Press; Hero et al. 2005Hero J-M, Williams SE, Magnusson WE (2005) Ecological traits of declining amphibians in upland areas of eastern Australia. Journal of Zoology 267:221-232. doi: 10.1017/S0952836905007296
https://doi.org/10.1017/S095283690500729... ). On the other hand, species with larger clutch size may present a higher ability to respond to climate change, for they present shorter life cycles (Mckinney 1997Mckinney ML (1997) EXTINCTION VULNERABILITY AND SELECTIVITY : Combining Ecological and Paleontological Views. 495-516). Larger clutch size is related to the probability of occupying broader geographic areas, higher dispersal ability and higher ability to colonise changing habitats and explore new opportunities (Duncan et al. 2001Duncan RP, Bomford M, Forsyth DM, Conibear L (2001) High predictability in introduction outcomes and the geographical range size of introduced Australian birds: a role for climate. Journal of Animal Ecology 70:621-632; Hero et al. 2005Hero J-M, Williams SE, Magnusson WE (2005) Ecological traits of declining amphibians in upland areas of eastern Australia. Journal of Zoology 267:221-232. doi: 10.1017/S0952836905007296
https://doi.org/10.1017/S095283690500729... ).

Some studies have found a significant relationship between clutch size and environmental variables. In temperate regions (with severe winter), studies with birds have shown that temperature increases have led to larger clutch sizes (Jarvinen 1996Jarvinen A (1996) Correlation between egg size and clutch size in the Pied Flycatcher Bicedula hypoleuca in cold and warm summers. Ibis 138:620-623; Przybylo et al. 2000Przybylo R, Sheldon BC, Merila J (2000) Climatic effects on breeding and morphology: evidence for phenotypic plasticity. Journal of Animal Ecology 69:395-403; Møller 2002Møller AP (2002) North Atlantic Oscillation (NAO) effects of climate on the relative importance of first and second clutches in a migratory passerine bird. Journal of Agricultural and Resource Economics 71:201-210; Husek and Adamík 2008Husek J, Adamík P (2008) Long-term trends in the timing of breeding and brood size in the Red-Backed Shrike Lanius collurio in the Czech Republic, 1964-2004. Journal of Ornithology 149:97-103. doi: 10.1007/s10336-007-0222-5
https://doi.org/10.1007/s10336-007-0222-... ; Table 1). The mechanism involved in this physiological adjustment seems to be related to resource availability. In these regions, the cold climate imposes food shortage (Jarvinen 1986Jarvinen A (1986) Clutch size of passerines in harsh environments. Oikos 46:365-371, 1996Jarvinen A (1996) Correlation between egg size and clutch size in the Pied Flycatcher Bicedula hypoleuca in cold and warm summers. Ibis 138:620-623), and higher temperatures lead to higher food availability, allowing species to have a higher number of broods. Annual variation in temperature, which reflects the seasonality of resources, was the most crucial variable to explain clutch size in a global assessment (Jetz et al. 2008Jetz W, Sekercioglu CH, Bohning-Gaese K (2008) The Worldwide Variation in Avian Clutch Size across Species and Space. PLoS Biology 6:e303. doi: 10.1371/journal.pbio.0060303
https://doi.org/10.1371/journal.pbio.006... ). For example, the clutch size of owls in Finland is strongly determined by the abundance of their prey (voles): warmer years, with thinner snow cover, favour a higher abundance of voles, allowing larger clutch size (Lehikoinen et al. 2011Lehikoinen A, Ranta E, Pietiäinen H, et al (2011) The impact of climate and cyclic food abundance on the timing of breeding and brood size in four boreal owl species. Oecologia 349-355. doi: 10.1007/s00442-010-1730-1
https://doi.org/10.1007/s00442-010-1730-... ). Such a positive relationship between food availability and mean clutch size in birds is well-known (Lack 1947Lack D (1947) The significance of clutch-size. Part I - Intraespecific variation. Ibis 89:302-352; Price 1985Price T (1985) Reproductive responses to varying food supply in a population of Darwin’s finches: Clutch size, growth rates and hatching synchrony. Oecologia 66:411-416; Gibbs and Grant 1987Gibbs HL, Grant PR (1987) ECOLOGICAL CONSEQUENCES OF AN EXCEPTIONALLY STRONG EL NINO EVENT ON DARWIN’S FINCHES. Ecology 68:1735-1746). Correlation between clutch size and climatic variables was also confirmed for other groups such as lizards (Smith et al. 1995Smith GR, Ballinger RE, Rose BR (1995) REPRODUCTION IN SCELOPORUS VIRGATUS FROM THE CHIRICAHUA MOUNTAINS OF SOUTHEASTERN ARIZONA WITH EMPHASIS ON ANNUAL VARIATION. Herpetologica 51:342-349; Abell 1999Abell AJ (1999) Variation in Clutch Size and Offspring Size Relative to Environmental Conditions in the Lizard Sceloporus virgatus. Journal of Herpetology 33:173-180) and butterflies (Karlsson and Wiklund 2005Karlsson B, Wiklund C (2005) Butterfly life history and temperature adaptations; dry open habitats select for increased fecundity and longevity. Journal of Animal Ecology 74:99-104. doi: 10.1111/j.1365-2656.2004.00902.x
https://doi.org/10.1111/j.1365-2656.2004... ; Saastamoinen 2007Saastamoinen M (2007) Life-history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly. Ecological Entomology 32:235-242). In this sense, for species that live in temperate regions, where the cold is a limiting factor for population regulation, climate change may positively impact environmental conditions, increase resource availability, and allow larger clutch size.

In the tropical region, resource seasonality is less intense, and the reproductive season is longer, which allow species to attempt reproduction more frequently per season (Martin, 1996Martin TE (1995) Avian Life History Evolution in Relation to Nest Sites, Nest Predation, and Food. Ecological Monographs 65:101-127). A higher number of attempts to reproduce may lead to smaller clutch size, as the parents need to save energy to invest in the next clutch (Slagsvold 1984Slagsvold T (1984) Clutch Size Variation of Birds in Relation to Nest Predation: On the Cost of Reproduction. Journal of Animal Ecology 53:945-953; Farnsworth and Simons 2001Farnsworth GL, Simons TR (2001) How many baskets? Clutch sizes that maximise annual fecundity of multiple-brooded birds. The Auk 118:973-982). This seems to be a good strategy in the tropics since nest predation is higher than in the temperate region, which would allow the spread of predation risk in numerous reproduction attempts (Cody 1966Cody ML (1966) A general theory of clutch size. Evolution 20:174-184; Kulesza 1990Kulesza G (1990) An analysis of clutch-size in New World passerine birds. Ibis 132:407-422; Martin 1995Martin TE (1995) Avian Life History Evolution in Relation to Nest Sites, Nest Predation, and Food. Ecological Monographs 65:101-127; Griebeler et al. 2010Griebeler EM, Caprano T, Bohning-Gaese K (2010) Evolution of avian clutch size along latitudinal gradients: do seasonality , nest predation or breeding season length matter? Journal of Evolutionary Biology 23:888-901. doi: 10.1111/j.1420-9101.2010.01958.x
https://doi.org/10.1111/j.1420-9101.2010... ; Table1). If clutch size depends on nest predation rate, as proposed by Skutch (1949)Skutch AF (1949) DO TROPICAL BIRDS REAR AS MANY YOUNG AS THEY CAN NOURISH? Ibis 91:430-455, if larger broods attract more predators, natural selection will favour smaller clutch sizes in the tropics (Martin et al. 2000Martin TE, Martin PR, Olson CR, et al (2000) Parental Care and Clutch Sizes in North and South American Birds. Science 287:1482-1485). Considering that, a possible consequence of climate change to species that inhabit the tropics is that temperature increase and rainfall decrease might shorten the reproductive season, leading to a reduction in the number of reproduction attempts, which could force species to compensate by increasing clutch size (Lovette and Fitzpatrick 2016Lovette IJ, Fitzpatrick JW (eds.) (2016) Handbook of bird biology. John Wiley & Sons, Hoboken, NJ). That would represent a risk for species since the tropics nest predation rate is relatively high, reaching 80-90% (revised by Stutchbury and Morton 2001Stutchbury BM, Morton ES (2001) Behavioral ecology of tropical birds. Academic Press, London, UK ).

In regions where climate change will cause temperature increase and significant rainfall decrease, making the areas arider, species tend to reduce the clutch size (Grant et al. 2000Grant PR, Grant BR, Keller LF, Petren K (2000) Effects of El Nino events on Darwin’s finch productivity. Ecology 81:2442-2457. doi: 10.1890/0012-9658(2000)081[2442:EOENOE]2.0.CO;2
https://doi.org/10.1890/0012-9658(2000)0... ; Coe and Rotenberry 2003Coe SJ, Rotenberry JT (2003) WATER AVAILABILITY AFFECTS CLUTCH SIZE IN A DESERT SPARROW. Ecology 84:3240-3249; Table 1). A study in the California desert has shown that, in territories that received water supplementation (treatment), a desert sparrow had a significantly larger clutch size than in non-supplemented territories (control) (Coe and Rotenberry 2003Coe SJ, Rotenberry JT (2003) WATER AVAILABILITY AFFECTS CLUTCH SIZE IN A DESERT SPARROW. Ecology 84:3240-3249). This result shows that environment variables have an indirect effect (regulating food availability) and act directly on physiology, so that supplemented females can allocate more water to egg production. During the reproductive period, females need a significantly higher amount of water to produce eggs since they contain a high percentage of water (Bartholomew and Cade 1963Bartholomew GA, Cade TJ (1963) The Water Economy of Land Birds. The American Naturalist 80:504-539; Reynolds and Waldron 1999Reynolds SJ, Waldron S (1999) Body water dynamics at the onset of egg-laying in the Zebra Finch Taeniopygia guttata. Journal of Avian Biology 30:1-6. doi: 10.2307/3677236
https://doi.org/10.2307/3677236... ).

Another hypothesis used to explain smaller clutch size in the tropical region than the temperate region is the egg-viability hypothesis (Stoleson and Beissinger 1999Stoleson SH, Beissinger SR (1999) Egg viability as a constraint on hatching synchrony at high ambient temperatures. Journal of Animal Ecology 68:951-962; Table 1). According to this hypothesis, in the tropics, where the temperature is higher, extended exposure of the eggs to temperatures higher than 24-26ºC (physiological zero) may trigger embryonic development even when the eggs are not incubated. Such premature development of the embryos below optimum incubation temperature (36-38ºC) results in abnormal growth of some tissues and consequent embryo death (Deeming and Ferguson 1992Deeming DC, Ferguson MWJ (1992) Physiological effects of incubation temperature on embryonic development in reptiles and birds. Egg incubation: its effects on embryonic development in birds and reptiles (eds DC Deeming & MWJ Ferguson), pp. 147±173. Cambridge University Press, Cambridge.; Stoleson 1999Stoleson SH (1999) The importance of the early onset of incubation for the maintenance of egg viability. Pages 600-613 in NJ Adams and RH Slotow (editors). Proceedings of the 22nd International Ornithological Congress. BirdLife South Africa, Johannesburg, South Africa). Therefore, birds that live in the tropics may lay smaller clutches to start active incubation earlier to keep the viability of the first eggs instead of waiting until many eggs are laid (Stoleson and Beissinger 1999Stoleson SH, Beissinger SR (1999) Egg viability as a constraint on hatching synchrony at high ambient temperatures. Journal of Animal Ecology 68:951-962). Based on this hypothesis, in a scenario of temperature increase, it is expected that species initiate incubation earlier and earlier to avoid loss of the first eggs, which can lead to smaller clutch size, since premature incubation or contact with the eggs may interrupt follicular growth and egg-laying (Haywood 1993Haywood S (1993) Sensory and hormonal control of clutch size in birds. Quarterly Review of Biology 68:33-51. doi: 10.1086/417910
https://doi.org/10.1086/417910... ).

Available evidence shows that species can adjust to climate change through phenotypic plasticity instead of altering their genetic constitution through microevolutionary adaptation (Gienapp et al. 2008Gienapp P, Teplitsky C, Alho JS, et al (2008) Climate change and evolution: disentangling environmental and genetic responses. Molecular Ecology 17:167-178. doi: 10.1111/j.1365-294X.2007.03413.x
https://doi.org/10.1111/j.1365-294X.2007... ). There seems to be low, or no additive genetic variation to clutch size and most intrapopulation variation is due to transitory environmental effects (Gibbs 1988Gibbs HL (1988) Heritability and selection on clutch size in darwin’s medium ground finches (Geospiza fortis). Evol 42:750-762). Species may present fast physiologic responses adjusting the clutch size to environmental changes (Gibbs 1988Gibbs HL (1988) Heritability and selection on clutch size in darwin’s medium ground finches (Geospiza fortis). Evol 42:750-762; Baker 1995Baker M (1995) Environmental Component of Latitudinal Clutch-Size Variation in House Sparrows (Passer domesticus). The Auk 112:249-252; Coe and Rotenberry 2003Coe SJ, Rotenberry JT (2003) WATER AVAILABILITY AFFECTS CLUTCH SIZE IN A DESERT SPARROW. Ecology 84:3240-3249). For example, the mean clutch size for sparrows in New York was 4.7 eggs, while in Costa Rica, it was two eggs (reviews in Baker 1995Baker M (1995) Environmental Component of Latitudinal Clutch-Size Variation in House Sparrows (Passer domesticus). The Auk 112:249-252). When sparrows captured in Costa Rica were raised in aviaries in New York, their clutch size was 3.50 (+ 0.46) eggs in the first year and 4.62 (+ 0.55) in the second year. Sparrows from New York raised in nearby aviaries under the same feeding conditions, and same pressures had a mean clutch size of 4.89 (+ 0.48) eggs (Baker 1995Baker M (1995) Environmental Component of Latitudinal Clutch-Size Variation in House Sparrows (Passer domesticus). The Auk 112:249-252). This example shows that species do not need several generations to adjust their clutch size to climatic conditions. Therefore, negative impacts on species that will be forced to reduce their clutch size, such as low population recruitment, could occur at a somewhat accelerated pace, thus increasing their vulnerability.

2. Diet breadth

In general, studies that assess climatic effects on diet are not focused on a specific taxon, but there is a prevalence of studies with vertebrates living in the temperate region (Table 2). Diet is an important trait that summarises distinct morphological, physiological and behavioural characteristics of a given organism, determining how it interacts with the biotic and abiotic environments (Donnell et al. 2012Donnell SO, Logan CJ, Clayton NS (2012) Specialisations of birds that attend army ant raids: An ecological approach to cognitive and behavioral studies. Behavioural Processes 91:267-274. doi: 10.1016/j.beproc.2012.09.007
https://doi.org/10.1016/j.beproc.2012.09... ; Abrahamczyk and Kessler 2014Abrahamczyk S, Kessler M (2014) Morphological and behavioural adaptations to feed on nectar : how feeding ecology determines the diversity and composition of hummingbird assemblages. Journal of Ornithology 156:333-347. doi: 10.1007/s10336-014-1146-5
https://doi.org/10.1007/s10336-014-1146-... ). It is expected that species with specialised diets present narrow niches, low local abundance and restricted geographic distribution (Mckinney 1997Mckinney ML (1997) EXTINCTION VULNERABILITY AND SELECTIVITY : Combining Ecological and Paleontological Views. 495-516). On the other hand, generalist species have flexible behaviour and can change their feeding habits to adapt to changes in resource availability (O’Donoghue et al. 1998O’Donoghue M, Boutin S, Krebs CJ, et al (1998) Functional responses of coyotes and lynx to the snowshoe hare cycle. Ecology 79:1193-1208. doi: 10.1890/0012-9658(1998)079[1193:FROCAL]2.0.CO;2
https://doi.org/10.1890/0012-9658(1998)0... ). Therefore, the diet breadth of a given species may influence its extinction risk (Boyles and Storm 2007Boyles JG, Storm JJ (2007) The Perils of Picky Eating: Dietary Breadth Is Related to Extinction Risk in Insectivorous Bats. PLoS ONE 2:e672. doi: 10.1371/journal.pone.0000672
https://doi.org/10.1371/journal.pone.000... ). Species with a more specialised diet are associated with higher probabilities of negative response to climate change (Pacifici et al. 2017Pacifici M, Visconti P, Butchart SHM, et al (2017) Species’ traits influenced their response to recent climate change. Nature Climate Change 7:205-208. doi: 10.1038/nclimate3223
https://doi.org/10.1038/nclimate3223... ). We will discuss three main mechanisms species may respond to climate change through their diets (Table 2).

Climate change may affect the availability of feeding resources. In regions where these resources will decrease, species with specialised diets will become more sensitive, presenting a higher extinction risk than generalist species (Chessman 2013Chessman BC (2013) Identifying species at risk from climate change: Traits predict the drought vulnerability of freshwater fishes. Biological Conservation 160:40-49. doi: 10.1016/j.biocon.2012.12.032
https://doi.org/10.1016/j.biocon.2012.12... ). Species with broader diet breadth can avoid hunger by changing their diet to the available food item during adverse climatic conditions (Brändle et al. 2002Brändle M, Prinzing A, Pfeifer R, Brandl R (2002) Dietary niche breadth for Central European birds: correlations with species-specific traits. Evolutionary Ecology Research 4:643-657). Such plasticity in the diet is a mechanism that has allowed species to deal with climate-related fluctuations in availability and abundance of resources (Furness 1996Furness RW (1996) A review of seabird responses to natural and fisheries-induced changes in food supply. In: Greenstreet SPR, Tasker ML (eds) Aquatic predators and their prey. Fishing News Books, Blackwell Science, Oxford, p 166−173; Ancona et al. 2012Ancona S, Calixto-Albarrán I, Drummond H (2012) Effect of El Niño on the diet of a specialist seabird, Sula nebouxii, in the warm eastern tropical Pacific. Marine Ecology Progress Series 462:261-271. doi: 10.3354/meps09851
https://doi.org/10.3354/meps09851... ). Generalist species can increase diet diversity in response to unfavourable changes in the weather when their preferred resources are scarce. They are led to supplement their diets with available resources at the moment (Folks et al. 2014Folks DJ, Gann K, Fulbright TE, et al (2014) Drought but not population density influences dietary niche breadth in white-tailed deer in a semiarid environment. Ecosphere 5:1-15. doi: 10.1890/ES14-00196.1
https://doi.org/10.1890/ES14-00196.1... ; Gray et al. 2016Gray EL, Burwell CJ, Baker AM (2016) Benefits of being a generalist carnivore when threatened by climate change: The comparative dietary ecology of two sympatric semelparous marsupials, including a new endangered species (Antechinus arktos). Australian Journal of Zoology 64:249-261. doi: 10.1071/ZO16044
https://doi.org/10.1071/ZO16044... ; Table 2). For example, temperature increase in North Pacific waters alters the availability of sea lion preys, making them change their diet, increasing the diversity of consumed preys (Robinson et al. 2018Robinson H, Thayer J, Sydeman WJ, Weise M (2018) Changes in California sea lion diet during a period of substantial climate variability. Marine Biology 165:1-12. doi: 10.1007/s00227-018-3424-x
https://doi.org/10.1007/s00227-018-3424-... ). In Northern Italy, owls have become more generalist under adverse climatic conditions: increased rainfall and decreased temperature increased the breadth of owls’ diets. (Rubolini et al. 2003Rubolini D, Pirovano A, Borghi S (2003) Influence of seasonality, temperature and rainfall on the winter diet of the long-eared owl, Asio otus. Folia Zoologica 52:67-76). Alternatively, species with specialised diets may not respond to resource fluctuation and therefore experience higher extinction risk. For mountain birds, temperature increase can result in population decrease caused by the abundance of preys, insects from the Tipulidae family adapted to cold weather (Pearce-Higgins 2010Pearce-Higgins JW (2010) Using diet to assess the sensitivity of northern and upland birds to climate change. Climate Research 45:119-130. doi: 10.3354/cr00920
https://doi.org/10.3354/cr00920... ). Temperature and rainfall increase during winter caused a significant decrease in the Eastern quoll population due to a reduction in the abundance of moth larvae (Fancourt et al. 2018Fancourt BA, Hawkins CE, Nicol SC (2018) Mechanisms of climate-change-induced species decline: spatial, temporal and long-term variation in the diet of an endangered marsupial carnivore, the eastern quoll. Wildlife Research 45:737-750. doi: 10.1071/WR18063
https://doi.org/10.1071/WR18063... ).

Diet type may influence species ability to change their phenologic events (Altermatt 2010Altermatt F (2010) Tell me what you eat and I’ll tell you when you fly: Diet can predict phenological changes in response to climate change. Ecology Letters 13:1475-1484. doi: 10.1111/j.1461-0248.2010.01534.x
https://doi.org/10.1111/j.1461-0248.2010... ) and their distribution area (Angert et al. 2011Angert AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecology Letters 14:677-689. doi: 10.1111/j.1461-0248.2011.01620.x
https://doi.org/10.1111/j.1461-0248.2011... ) to follow climate change. Species that are not able to change their distribution areas fast enough to follow their adequate climatic conditions are at higher risk of extinction (Devictor et al. 2008Devictor V, Julliard R, Couvet D, Jiguet F (2008) Birds are tracking climate warming, but not fast enough. Proceedings Biological sciences / The Royal Society 275:2743-2748. doi: 10.1098/rspb.2008.0878
https://doi.org/10.1098/rspb.2008.0878... ), as well as those species that cannot change phenology to match species that they depend on for survival (Visser and Both 2005Visser ME, Both C (2005) Shifts in phenology due to global climate change: The need for a yardstick. Proceedings of the Royal Society B: Biological Sciences 272:2561-2569. doi: 10.1098/rspb.2005.3356
https://doi.org/10.1098/rspb.2005.3356... ). Generally, diet generalists are expected to be more likely to find adequate resources in new areas. They should, therefore, present a greater ability to change their distributions than specialists, which could be more limited by the phenology of species they depend on (Angert et al. 2011Angert AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecology Letters 14:677-689. doi: 10.1111/j.1461-0248.2011.01620.x
https://doi.org/10.1111/j.1461-0248.2011... ; Buckley and Kingsolver 2012Buckley LB, Kingsolver JG (2012) Functional and Phylogenetic Approaches to Forecasting Species’ Responses to Climate Change. Annual Review of Ecology, Evolution, and Systematics 205-226. doi: 10.1146/annurev-ecolsys-110411-160516
https://doi.org/10.1146/annurev-ecolsys-... ). Broader diets can facilitate the expansion of distribution areas driven by climate (Braschler and Hill 2007Braschler B, Hill JK (2007) Role of larval host plants in the climate-driven range expansion of the butterfly Polygonia c-album. Journal of Animal Ecology 76:415-423. doi: 10.1111/j.1365-2656.2007.01217.x
https://doi.org/10.1111/j.1365-2656.2007... ) and the establishment and persistence of species in new environments (Estrada et al. 2016Estrada A, Morales-castilla I, Caplat P, Early R (2016) Usefulness of Species Traits in Predicting Range Shifts. Trends in Ecology & Evolution 31:190-203. doi: 10.1016/j.tree.2015.12.014
https://doi.org/10.1016/j.tree.2015.12.0... ). However, a specialist may have a greater probability of following spatial changes if its host species or prey also changes (Betzholtz et al. 2013Betzholtz PE, Pettersson LB, Ryrholm N, Franzén M (2013) With that diet, you will go far: Trait-based analysis reveals a link between rapid range expansion and a nitrogen-favoured diet. Proceedings of the Royal Society B: Biological Sciences 280:. doi: 10.1098/rspb.2012.2305
https://doi.org/10.1098/rspb.2012.2305... ; Auer and King 2014Auer SK, King DI (2014) Ecological and life-history traits explain recent boundary shifts in elevation and latitude of western North American songbirds. Global Ecology and Biogeography 23:867-875. doi: 10.1111/geb.12174
https://doi.org/10.1111/geb.12174... ). Generally, diet specialists could be more affected by climate change since they present narrower distribution, are less likely to leave their habitats (Caldas 2014Caldas A (2014) Species Traits of Relevance for Climate Vulnerability and the Prediction of Phenological Responses to Climate Change. Journal of the Lepidopterists’ Society 68:197-202) and alter their phenologic events (Altermatt 2010Altermatt F (2010) Tell me what you eat and I’ll tell you when you fly: Diet can predict phenological changes in response to climate change. Ecology Letters 13:1475-1484. doi: 10.1111/j.1461-0248.2010.01534.x
https://doi.org/10.1111/j.1461-0248.2010... ) to track adequate climatic conditions.

The temperature increase may cause omnivore species to change their diet, becoming more herbivores and fewer carnivores (Table 2). For ectotherms, low body temperature makes herbivory energetically unfavourable, as it constrains the rate at which energy can be extracted from the diet (Floeter et al. 2005Floeter SR, Behrens MD, Ferreira CEL, et al (2005) Geographical gradients of marine herbivorous fishes: patterns and processes. Marine Biology 147:1435-1447. doi: 10.1007/s00227-005-0027-0
https://doi.org/10.1007/s00227-005-0027-... ; Boersma et al. 2016Boersma M, Mathew KA, Niehoff B, et al (2016) Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it’s hot? Ecology Letters 19:45-53. doi: 10.1111/ele.12541
https://doi.org/10.1111/ele.12541... ). For marine herbivorous fishes, herbivory is only possible above a threshold of 15°C (Floeter et al. 2005Floeter SR, Behrens MD, Ferreira CEL, et al (2005) Geographical gradients of marine herbivorous fishes: patterns and processes. Marine Biology 147:1435-1447. doi: 10.1007/s00227-005-0027-0
https://doi.org/10.1007/s00227-005-0027-... ). There seems to be a consensus that due to better digestion of vegetal material at high temperatures, ectotherms might maximise energy intake and maintain high metabolic rates in higher temperatures by increasing herbivory (Carreira et al. 2016Carreira BM, Segurado P, Orizaola G, et al (2016) Warm vegetarians? Heat waves and diet shifts in tadpoles. Ecological Monographs 97:2964-2974. doi: 10.1002/ecy.1541
https://doi.org/10.1002/ecy.1541... ). This idea is supported by studies that have found that herbivory increases in response to higher temperatures in several groups, such as Copepoda (Boersma et al. 2016Boersma M, Mathew KA, Niehoff B, et al (2016) Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it’s hot? Ecology Letters 19:45-53. doi: 10.1111/ele.12541
https://doi.org/10.1111/ele.12541... ), fish (Floeter et al. 2005Floeter SR, Behrens MD, Ferreira CEL, et al (2005) Geographical gradients of marine herbivorous fishes: patterns and processes. Marine Biology 147:1435-1447. doi: 10.1007/s00227-005-0027-0
https://doi.org/10.1007/s00227-005-0027-... ), tadpoles (Carreira et al. 2016Carreira BM, Segurado P, Orizaola G, et al (2016) Warm vegetarians? Heat waves and diet shifts in tadpoles. Ecological Monographs 97:2964-2974. doi: 10.1002/ecy.1541
https://doi.org/10.1002/ecy.1541... ) and reptiles (Espinoza et al. 2004Espinoza RE, Wiens JJ, Tracy CR (2004) Recurrent evolution of herbivory in small, cold-climate lizards: Breaking the ecophysiological rules of reptilian herbivory. Proceedings of the National Academy of Sciences 101:16819-16824. doi: 10.1073/pnas.0401226101
https://doi.org/10.1073/pnas.0401226101... ). Even amongst endotherms, herbivores maintain higher body temperature than carnivores (Clarke and O’Connor 2014Clarke A, O’Connor MI (2014) Diet and body temperature in mammals and birds. Global Ecology and Biogeography 23:1000-1008. doi: 10.1111/geb.12185
https://doi.org/10.1111/geb.12185... ). Although omnivores can regulate their diet to deal with temperature increase caused by climate change, changing to a more herbivore diet and its adaptive value is variable among species (Carreira et al. 2016Carreira BM, Segurado P, Orizaola G, et al (2016) Warm vegetarians? Heat waves and diet shifts in tadpoles. Ecological Monographs 97:2964-2974. doi: 10.1002/ecy.1541
https://doi.org/10.1002/ecy.1541... ). Besides, an increase in herbivory in response to global warming can alter food chains, species interactions, and ecosystems’ functioning.

3. Dispersal ability

Birds and lepidopterans are the best-represented taxa in studies regarding climatic effects on dispersal ability, and no studies were carried out in the tropical region (Table 3). Understanding species ability to respond to climate change is a fundamental point to identify species that experience higher risk (Møller et al. 2008Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences 105:16195-16200. doi: 10.1073/pnas.0803825105
https://doi.org/10.1073/pnas.0803825105... ; Hurlbert and Liang 2012Hurlbert AH, Liang Z (2012) Spatiotemporal Variation in Avian Migration Phenology: Citizen Science Reveals Effects of Climate Change. PLoS ONE 7:e31662. doi: 10.1371/journal.pone.0031662
https://doi.org/10.1371/journal.pone.003... ). Species that cannot change their annual cycles and their distributions to follow their suitable climatic conditions will be prone to higher extinction risk (Møller et al. 2008Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences 105:16195-16200. doi: 10.1073/pnas.0803825105
https://doi.org/10.1073/pnas.0803825105... ; Corlett and Westcott 2013Corlett RT, Westcott DA (2013) Will plant movements keep up with climate change? Trends in Ecology & Evolution 28:482-488. doi: 10.1016/j.tree.2013.04.003
https://doi.org/10.1016/j.tree.2013.04.0... ). In this sense, dispersal ability is a crucial attribute for species. It is expected that those with higher dispersal ability respond more quickly to climate change, presenting lower extinction risk (Pöyry et al. 2009Pöyry J, Luoto M, Heikkinen R, et al (2009) Species traits explain recent range shifts of Finnish butterflies. Global Change Biology 15:732-743. doi: 10.1111/j.1365-2486.2008.01789.x
https://doi.org/10.1111/j.1365-2486.2008... ; Angert et al. 2011Angert AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecology Letters 14:677-689. doi: 10.1111/j.1461-0248.2011.01620.x
https://doi.org/10.1111/j.1461-0248.2011... ).

Climate change can affect the dispersal processes of organisms both directly and indirectly (Travis et al. 2013Travis JMJ, Delgado M, Bocedi G, et al (2013) Dispersal and species’ responses to climate change. Oikos 122:1532-1540. doi: 10.1111/j.1600-0706.2013.00399.x
https://doi.org/10.1111/j.1600-0706.2013... ; Table 3). Indirect mechanisms (e.g. altering resource availability and climatic suitability of the habitat) may lead species to change their distribution areas. Their annual cycles will be discussed in the following paragraphs (Table 3). On the other hand, climate change may directly interfere with behaviour, affecting the organisms’ decisions to stimulate or inhibit dispersal (Table 3). Higher temperatures increase the dispersal of moths (Battisti et al. 2006Battisti A, Stastny M, Buffo E, Larsson S (2006) A rapid altitudinal range expansion in the pine processionary moth produced by the 2003 climatic anomaly. Global Change Biology 12:662-671. doi: 10.1111/j.1365-2486.2006.01124.x
https://doi.org/10.1111/j.1365-2486.2006... ), butterflies (Cormont et al. 2011Cormont A, Malinowska AH, Kostenko O, et al (2011) Effect of local weather on butterfly flight behaviour, movement, and colonisation: significance for dispersal under climate change. Biodiversity and Conservation 20:483-503. doi: 10.1007/s10531-010-9960-4
https://doi.org/10.1007/s10531-010-9960-... ) and birds (Møller et al. 2006Møller AP, Flensted-Jensen E, Mardal W (2006) Dispersal and climate change: a case study of the Arctic tern Sterna paradisaea. Global Change Biology 12:2005-2013. doi: 10.1111/j.1365-2486.2006.01216.x
https://doi.org/10.1111/j.1365-2486.2006... ) and decrease dispersal of lizards (Massot et al. 2008Massot M, Clobert J, Ferrière R (2008) Climate warming, dispersal inhibition and extinction risk. Global Change Biology 14:461-469. doi: 10.1111/j.1365-2486.2007.01514.x
https://doi.org/10.1111/j.1365-2486.2007... ). Flooding increases the dispersal of an aquatic bird in Canada (Roche et al. 2012Roche EA, Gratto-Trevor CL, Goossen JP, White CL (2012) FLOODING AFFECTS DISPERSAL DECISIONS IN PIPING PLOVERS (CHARADRIUS MELODUS) IN PRAIRIE CANADA. The Auk 129:296-306. doi: 10.1525/auk.2012.11196
https://doi.org/10.1525/auk.2012.11196... ), and the reduction of snow cover decreases the dispersal of wolverines in the USA (Schwartz et al. 2009Schwartz MK, Copeland JP, Anderson NJ, et al (2009) Wolverine Gene Flow across a Narrow Climatic Niche. Ecology 90:3222-3232). These examples indicate that climatic variables may increase or reduce dispersal depending on the system and the species (Travis et al. 2013Travis JMJ, Delgado M, Bocedi G, et al (2013) Dispersal and species’ responses to climate change. Oikos 122:1532-1540. doi: 10.1111/j.1600-0706.2013.00399.x
https://doi.org/10.1111/j.1600-0706.2013... ). Moreover, species response may depend on weather and landscape configuration (Delattre et al. 2013Delattre T, Baguette M, Burel F, et al (2013) Interactive effects of landscape and weather on dispersal. Oikos 122:1576-1585. doi: 10.1111/j.1600-0706.2013.00123.x
https://doi.org/10.1111/j.1600-0706.2013... ). In more fragmented landscapes, dispersal distance is longer at lower temperatures, while in continuous landscapes, dispersal distance is longer at higher temperatures.

Recent climate change is quickly altering the location of areas with a suitable climate for certain species (Loarie et al. 2009Loarie SR, Duffy PB, Hamilton H, et al (2009) The velocity of climate change. Nature 462:1052-1055. doi: 10.1038/nature08649
https://doi.org/10.1038/nature08649... ). To survive, species must move fast enough to follow such changes (Chen et al. 2011Chen I, Hill JK, Ohlemüller R, et al (2011) Rapid range shifts of species of climate warming. Science 333:1024-1026. doi: 10.1126/science.1206432
https://doi.org/10.1126/science.1206432... ; Lenoir and Svenning 2015Lenoir J, Svenning J (2015) Climate-related range shifts - a global multidimensional synthesis and new research directions. Ecography 38:15-28. doi: 10.1111/ecog.00967
https://doi.org/10.1111/ecog.00967... ). Therefore, as expected for the future, climate change might be a significant threat to species persistence since rates of distribution changes should be much higher than those observed in the past (Williams and Blois 2018Williams JE, Blois JL (2018) Range shifts in response to past and future climate change: Can climate velocities and species’ dispersal capabilities explain variation in mammalian range shifts? Journal of Biogeography 45:2175-2189. doi: 10.1111/jbi.13395
https://doi.org/10.1111/jbi.13395... ). Some studies show that many organisms will not be able to disperse fast enough to follow their climatic niches, even highly mobile species (Pearson 2006Pearson RG (2006) Climate change and the migration capacity of species. Trends in Ecology and Evolution 21:111-113. doi: 10.1016/j.tree.2005.11.022
https://doi.org/10.1016/j.tree.2005.11.0... ; Devictor et al. 2008Devictor V, Julliard R, Couvet D, Jiguet F (2008) Birds are tracking climate warming, but not fast enough. Proceedings Biological sciences / The Royal Society 275:2743-2748. doi: 10.1098/rspb.2008.0878
https://doi.org/10.1098/rspb.2008.0878... , 2012Devictor V, Van Swaay C, Brereton T, et al (2012) Differences in the climatic debts of birds and butterflies at a continental scale. Nature Climate Change 2:121-124. doi: 10.1038/nclimate1347
https://doi.org/10.1038/nclimate1347... ; Schloss et al. 2012Schloss CA, Nuñez TA, Lawler JJ (2012) Dispersal will limit ability of mammals to track climate change in the Western Hemisphere. Proceedings of the National Academy of Sciences of the United States of America 109:8606-8611. doi: 10.1073/pnas.1116791109
https://doi.org/10.1073/pnas.1116791109... ). Species with low dispersal ability might lose significant parts of their distribution areas in the future (Krause et al. 2015Krause CM, Cobb NS, Pennington DD (2015) Range Shifts Under Future Scenarios of Climate Change: Dispersal Ability Matters for Colorado Plateau Endemic Plants. Natural Areas Journal 35:428-438. doi: 10.3375/043.035.0306
https://doi.org/10.3375/043.035.0306... ), hence facing higher extinction risk (Pearson 2006Pearson RG (2006) Climate change and the migration capacity of species. Trends in Ecology and Evolution 21:111-113. doi: 10.1016/j.tree.2005.11.022
https://doi.org/10.1016/j.tree.2005.11.0... ; Corlett and Westcott 2013Corlett RT, Westcott DA (2013) Will plant movements keep up with climate change? Trends in Ecology & Evolution 28:482-488. doi: 10.1016/j.tree.2013.04.003
https://doi.org/10.1016/j.tree.2013.04.0... ). Therefore, dispersal ability is a good predictor of species vulnerability to climate change. Both empirical observations (Warren et al. 2001Warren MS, Hill JK, Thomas JA, et al (2001) Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414:65-69; Hill et al. 2002Hill JK, Thomas CD, Fox R, et al (2002) Responses of butterflies to twentieth century climate warming: implications for future ranges. Proceedings of the Royal Society B: Biological Sciences 269:2163-2171. doi: 10.1098/rspb.2002.2134
https://doi.org/10.1098/rspb.2002.2134... ; Pöyry et al. 2009Pöyry J, Luoto M, Heikkinen R, et al (2009) Species traits explain recent range shifts of Finnish butterflies. Global Change Biology 15:732-743. doi: 10.1111/j.1365-2486.2008.01789.x
https://doi.org/10.1111/j.1365-2486.2008... ; Angert et al. 2011Angert AL, Crozier LG, Rissler LJ, et al (2011) Do species’ traits predict recent shifts at expanding range edges? Ecology Letters 14:677-689. doi: 10.1111/j.1461-0248.2011.01620.x
https://doi.org/10.1111/j.1461-0248.2011... ) and model projections (Krause et al. 2015Krause CM, Cobb NS, Pennington DD (2015) Range Shifts Under Future Scenarios of Climate Change: Dispersal Ability Matters for Colorado Plateau Endemic Plants. Natural Areas Journal 35:428-438. doi: 10.3375/043.035.0306
https://doi.org/10.3375/043.035.0306... ; Methorst et al. 2017Methorst J, Böhning-Gaese K, Khaliq I, Hof C (2017) A framework integrating physiology, dispersal and land-use to project species ranges under climate change. Journal of Avian Biology 48:1532-1548. doi: 10.1111/jav.01299
https://doi.org/10.1111/jav.01299... ; Williams and Blois 2018Williams JE, Blois JL (2018) Range shifts in response to past and future climate change: Can climate velocities and species’ dispersal capabilities explain variation in mammalian range shifts? Journal of Biogeography 45:2175-2189. doi: 10.1111/jbi.13395
https://doi.org/10.1111/jbi.13395... ) evidence that higher dispersal ability indicates higher ability to change distribution to follow climate displacement (Table 3).

Recent global warming has already caused significant changes in many species’ life cycles (Walther et al. 2002Walther G, Post E, Convey P, et al (2002) Ecological responses to recent climate change. Nature 389-395; Parmesan and Yohe 2003Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42. doi: 10.1038/nature01286
https://doi.org/10.1038/nature01286... ). Generally, plants and animals have advanced their phenologies in response to temperature increase (Parmesan and Yohe 2003Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37-42. doi: 10.1038/nature01286
https://doi.org/10.1038/nature01286... ; Parmesan 2006Parmesan C (2006) Ecological and Evolutionary Responses to Recent Climate Change. Annual Review of Ecology, Evolution, and Systematics 37:637-669. doi: 10.1146/annurev.ecolsys.37.091305.110100
https://doi.org/10.1146/annurev.ecolsys.... ). However, consumers and predators at higher trophic levels in the food chain might not respond in the same proportion, leading to a mismatch between reproductive period and resource availability (Visser et al. 1998Visser ME, Noordwijk AJ Van, Tinbergen JM, Lessells CM (1998) Warmer springs lead to mistimed reproduction in great tits (Parus major). Proceedings of the Royal Society B: Biological Sciences 265:1867-1870, 2004Visser ME, Both C, Lambrechts MM (2004) Global Climate Change Leads to Mistimed Avian Reproduction. Advances in Ecological Research 35:89-110. doi: 10.1016/S0065-2504(04)35005-1
https://doi.org/10.1016/S0065-2504(04)35... ; Visser and Both 2005Visser ME, Both C (2005) Shifts in phenology due to global climate change: The need for a yardstick. Proceedings of the Royal Society B: Biological Sciences 272:2561-2569. doi: 10.1098/rspb.2005.3356
https://doi.org/10.1098/rspb.2005.3356... ). Species that cannot advance their arrival to reproduction sites to match the peak of food abundance may suffer population declines and, consequently, be more prone to extinction (Both et al. 2006Both C, Bouwhuis S, Lessells CM, Visser ME (2006) Climate change and population declines in a long-distance migratory bird. Nature 441:81-83. doi: 10.1038/nature04539
https://doi.org/10.1038/nature04539... ; Møller et al. 2008Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences 105:16195-16200. doi: 10.1073/pnas.0803825105
https://doi.org/10.1073/pnas.0803825105... ).

Migratory birds should advance the beginning of the migration to follow the phenology of plants and invertebrates in their reproduction areas (Sparks et al. 2005Sparks TH, Bairlein F, Bojarinova JG, et al (2005) Examining the total arrival distribution of migratory birds. Global Change Biology 11:22-30. doi: 10.1111/j.1365-2486.2004.00887.x
https://doi.org/10.1111/j.1365-2486.2004... ). Indeed, as a response to temperature increase in the last years, migratory birds have arrived earlier in their reproduction sites (Butler 2003Butler CJ (2003) The disproportionate effect of global warming on the arrival dates of short-distance migratory birds in North America. Ibis 145:484-495; Hurlbert and Liang 2012Hurlbert AH, Liang Z (2012) Spatiotemporal Variation in Avian Migration Phenology: Citizen Science Reveals Effects of Climate Change. PLoS ONE 7:e31662. doi: 10.1371/journal.pone.0031662
https://doi.org/10.1371/journal.pone.003... ). However, literature shows that long-distance migrants cannot respond to climatic change as quickly as short-distance migrants do and arrive later (Table 3). This happens because long-distance migrants experience slower temperature increase in wintering areas than their reproduction areas, while short-distance migrants are exposed to warm weather throughout the year (Lehikoinen et al. 2004Lehikoinen E, Sparks TH, Zalakevicius M (2004) Arrival and departure dates. Advances in Ecological Research 2504:. doi: 10.1016/S0065-2504(04)35001-4
https://doi.org/10.1016/S0065-2504(04)35... ). Therefore, short-distance migrants have more and better cues to match their phenology with resource phenology (Jones and Cresswell 2010Jones T, Cresswell W (2010) The phenology mismatch hypothesis: are declines of migrant birds linked to uneven global climate change? Journal of Animal Ecology 79:98-108. doi: 10.1111/j.1365-2656.2009.01610.x
https://doi.org/10.1111/j.1365-2656.2009... ). Thus, long-distance migratory behaviour can represent an essential constraint to responses to climate change, contributing to the decline of some species (Berthold et al. 1998Berthold P, Fiedler W, Schlenker R, Querner U (1998) 25Year Study of the Population Development of Central European Songbirds: A General Decline, Most Evident in Long-Distance Migrants. Naturwissenschaften 85:350-353. doi: 10.1007/s001140050514
https://doi.org/10.1007/s001140050514... ; Møller et al. 2008Møller AP, Rubolini D, Lehikoinen E (2008) Populations of migratory bird species that did not show a phenological response to climate change are declining. Proceedings of the National Academy of Sciences 105:16195-16200. doi: 10.1073/pnas.0803825105
https://doi.org/10.1073/pnas.0803825105... ; Jones and Cresswell 2010Jones T, Cresswell W (2010) The phenology mismatch hypothesis: are declines of migrant birds linked to uneven global climate change? Journal of Animal Ecology 79:98-108. doi: 10.1111/j.1365-2656.2009.01610.x
https://doi.org/10.1111/j.1365-2656.2009... ; Rubolini et al. 2010Rubolini D, Saino N, Møller AP (2010) Migratory behaviour constrains the phenological response of birds to climate change. Climate Research 42:45-55. doi: 10.3354/cr00862
https://doi.org/10.3354/cr00862... ).

4. Climatic tolerance

Studies assessing species climatic tolerance are focused on ectotherms, and most of them were carried out on a global scale (Table 4). Tolerance to climatic conditions is one of the most critical factors determining how species are distributed around the globe (Thomas 2010Thomas CD (2010) Climate, climate change and range boundaries. Diversity and Distributions 16:488-495. doi: 10.1111/j.1472-4642.2010.00642.x
https://doi.org/10.1111/j.1472-4642.2010... ). A variation in climatic tolerance among species is an important characteristic to determine their responses to climate change, as it can alter distribution and survival (Deutsch et al. 2008Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... ; Huey et al. 2012Huey RB, Kearney MR, Krockenberger A, et al (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B: Biological Sciences 367:1665-1679. doi: 10.1098/rstb.2012.0005
https://doi.org/10.1098/rstb.2012.0005... ; Caldwell et al. 2015Caldwell AJ, While GM, Beeton NJ, Wapstra E (2015) Potential for thermal tolerance to mediate climate change effects on three members of a cool temperate lizard genus, Niveoscincus. Journal of Thermal Biology 52:14-23. doi: 10.1016/j.jtherbio.2015.05.002
https://doi.org/10.1016/j.jtherbio.2015.... ; Rugiu et al. 2018Rugiu L, Manninen I, Sjöroos J, Jormalainen V (2018) Variations in tolerance to climate change in a key littoral herbivore. Marine Biology 165:1-11. doi: 10.1007/s00227-017-3275-x
https://doi.org/10.1007/s00227-017-3275-... ). Species with higher thermic tolerance occupy broader geographic areas (Bozinovic et al. 2011Bozinovic F, Calosi P, Spicer JI (2011) Physiological Correlates of Geographic Range in Animals. Annual Review of Ecology, Evolution and Systematics 42:155-179. doi: 10.1146/annurev-ecolsys-102710-145055
https://doi.org/10.1146/annurev-ecolsys-... ) and will deal better with global warming (Calosi et al. 2008Calosi P, Bilton DT, Spicer JI (2008) Thermal tolerance, acclimatory capacity and vulnerability to global climate change. Biology Letters 4:99-102. doi: 10.1098/rsbl.2007.0408
https://doi.org/10.1098/rsbl.2007.0408... ; Buckley et al. 2012Buckley LB, Kingsolver JG (2012) Functional and Phylogenetic Approaches to Forecasting Species’ Responses to Climate Change. Annual Review of Ecology, Evolution, and Systematics 205-226. doi: 10.1146/annurev-ecolsys-110411-160516
https://doi.org/10.1146/annurev-ecolsys-... ; Huey et al. 2012Huey RB, Kearney MR, Krockenberger A, et al (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B: Biological Sciences 367:1665-1679. doi: 10.1098/rstb.2012.0005
https://doi.org/10.1098/rstb.2012.0005... ). In general, the thermic tolerance of an organism is proportional to the magnitude of temperature variation experienced in its habitat, steeply increasing with latitude (Deutsch et al. 2008Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... ). Thus, species from the tropics, which inhabit environments with lower temperature variation throughout the year, have narrower thermic tolerance than species from temperate regions (Deutsch et al. 2008Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... ; Huey et al. 2009Huey RB, Deutsch CA, Tewksbury JJ, et al (2009) Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society B: Biological Sciences 276:1939-1948. doi: 10.1098/rspb.2008.19
https://doi.org/10.1098/rspb.2008.19... , 2012Huey RB, Kearney MR, Krockenberger A, et al (2012) Predicting organismal vulnerability to climate warming: roles of behaviour, physiology and adaptation. Philosophical Transactions of the Royal Society B: Biological Sciences 367:1665-1679. doi: 10.1098/rstb.2012.0005
https://doi.org/10.1098/rstb.2012.0005... ; Duarte et al. 2012Duarte H, Tejedo M, Katzenberger M, et al (2012) Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Global Change Biology 18:412-421. doi: 10.1111/j.1365-2486.2011.02518.x
https://doi.org/10.1111/j.1365-2486.2011... ; Khaliq et al. 2014Khaliq I, Hof C, Prinzinger R, et al (2014) Global variation in thermal tolerances and vulnerability of endotherms to climate change. Proceedings of the Royal Society B: Biological Sciences 281:20141097. doi: 10.1098/rspb.2014.1097
https://doi.org/10.1098/rspb.2014.1097... ; Table 4). Deutsch et al. (2008)Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... have reported that heat tolerance in tropical insects is, on average, only one-fifth of the tolerance of insect species from temperate regions. Besides that, tropical species already live in warmer environments, close to their critical temperature, compared to species from the temperate areas, which live in colder environments, far from their critical temperature (Sunday et al. 2012Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nature Climate Change 2:686-690. doi: 10.1038/nclimate1539
https://doi.org/10.1038/nclimate1539... ; Araújo et al. 2013Araújo MB, Ferri-Yáñez F, Bozinovic F, et al (2013) Heat freezes niche evolution. Ecology Letters 16:1206-1219. doi: 10.1111/ele.12155
https://doi.org/10.1111/ele.12155... ; Khaliq et al. 2014Khaliq I, Hof C, Prinzinger R, et al (2014) Global variation in thermal tolerances and vulnerability of endotherms to climate change. Proceedings of the Royal Society B: Biological Sciences 281:20141097. doi: 10.1098/rspb.2014.1097
https://doi.org/10.1098/rspb.2014.1097... ). Therefore, even slight temperature increases might be a threat to tropical species.

Heat tolerance is more conserved amongst lineages than cold tolerance, implying that many species might have lost their evolutionary potential to respond to global warming (Addo-Bediako et al. 2000Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society B: Biological Sciences 267:739-745; Huey et al. 2009Huey RB, Deutsch CA, Tewksbury JJ, et al (2009) Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society B: Biological Sciences 276:1939-1948. doi: 10.1098/rspb.2008.19
https://doi.org/10.1098/rspb.2008.19... ; Araújo et al. 2013Araújo MB, Ferri-Yáñez F, Bozinovic F, et al (2013) Heat freezes niche evolution. Ecology Letters 16:1206-1219. doi: 10.1111/ele.12155
https://doi.org/10.1111/ele.12155... ). When organisms are exposed to temperatures close to their upper thermal limit, biological activity suffers from several limitations and might compromise survival (Somero 2011Somero GN (2011) Comparative physiology: a “crystal ball” for predicting consequences of global change. American Journal of Physiology: Regulatory, Integrative and Comparative Physiology 301:R1-R14. doi: 10.1152/ajpregu.00719.2010.
https://doi.org/10.1152/ajpregu.00719.20... ). Furthermore, it is unlikely that species can persist under conditions that surpass their physiological tolerance limits (Calosi et al. 2010Calosi P, Bilton DT, Spicer JI, et al (2010) What determines a species’ geographical range? Thermal biology and latitudinal range size relationships in European diving beetles (Coleoptera: Dytiscidae). Journal of Animal Ecology 79:194-204. doi: 10.1111/j.1365-2656.2009.01611.x
https://doi.org/10.1111/j.1365-2656.2009... ). Thus, climatic conditions expected in the future might negatively affect population abundance and potentially compromise their persistence (Rugiu et al. 2018Rugiu L, Manninen I, Sjöroos J, Jormalainen V (2018) Variations in tolerance to climate change in a key littoral herbivore. Marine Biology 165:1-11. doi: 10.1007/s00227-017-3275-x
https://doi.org/10.1007/s00227-017-3275-... ). However, while tropical species might be severely affected, species from temperate regions might benefit from temperature increase, responding with higher population growth rates and aptitude (Deutsch et al. 2008Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... ; Caldwell et al. 2015Caldwell AJ, While GM, Beeton NJ, Wapstra E (2015) Potential for thermal tolerance to mediate climate change effects on three members of a cool temperate lizard genus, Niveoscincus. Journal of Thermal Biology 52:14-23. doi: 10.1016/j.jtherbio.2015.05.002
https://doi.org/10.1016/j.jtherbio.2015.... ; Carrascal et al. 2016Carrascal LM, Villén-Pérez S, Palomino D (2016) Preferred temperature and thermal breadth of birds wintering in peninsular Spain: the limited effect of temperature on species distribution. PeerJ 4:e2156. doi: 10.7717/peerj.2156
https://doi.org/10.7717/peerj.2156... ; Table 4).

Such pattern of greater physiological vulnerability to climatic changes in tropical species, when compared to species from temperate areas, has been shown to ectotherms, especially reptiles (Deutsch et al. 2008Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... ; Tewksbury et al. 2008Tewksbury JJ, Huey RB, Deutsch CA (2008) Putting the Heat on Tropical Animals The Scale of Prediction. Science 320:1296-1297. doi: 10.1126/science.1159328
https://doi.org/10.1126/science.1159328... ; Huey et al. 2009Huey RB, Deutsch CA, Tewksbury JJ, et al (2009) Why tropical forest lizards are vulnerable to climate warming. Proceedings of the Royal Society B: Biological Sciences 276:1939-1948. doi: 10.1098/rspb.2008.19
https://doi.org/10.1098/rspb.2008.19... , 2010Huey RB, Losos JB, Moritz C (2010) Are Lizards Toast? Science 328:832-833. doi: 10.1126/science.1190374
https://doi.org/10.1126/science.1190374... ; Diamond et al. 2012Diamond SE, Sorger DM, Hulcr J, et al (2012) Who likes it hot? A global analysis of the climatic, ecological, and evolutionary determinants of warming tolerance in ants. Global Change Biology 18:448-456. doi: 10.1111/j.1365-2486.2011.02542.x
https://doi.org/10.1111/j.1365-2486.2011... ; Duarte et al. 2012Duarte H, Tejedo M, Katzenberger M, et al (2012) Can amphibians take the heat? Vulnerability to climate warming in subtropical and temperate larval amphibian communities. Global Change Biology 18:412-421. doi: 10.1111/j.1365-2486.2011.02518.x
https://doi.org/10.1111/j.1365-2486.2011... ; Sunday et al. 2012Sunday JM, Bates AE, Dulvy NK (2012) Thermal tolerance and the global redistribution of animals. Nature Climate Change 2:686-690. doi: 10.1038/nclimate1539
https://doi.org/10.1038/nclimate1539... ; Hoffmann et al. 2013Hoffmann AA, Chown SL, Clusella-Trullas S (2013) Upper thermal limits in terrestrial ectotherms: How constrained are they? Functional Ecology 27:934-949. doi: 10.1111/j.1365-2435.2012.02036.x
https://doi.org/10.1111/j.1365-2435.2012... ; Caldwell et al. 2015Caldwell AJ, While GM, Beeton NJ, Wapstra E (2015) Potential for thermal tolerance to mediate climate change effects on three members of a cool temperate lizard genus, Niveoscincus. Journal of Thermal Biology 52:14-23. doi: 10.1016/j.jtherbio.2015.05.002
https://doi.org/10.1016/j.jtherbio.2015.... ). For endotherms, on the other hand, the relationship between higher thermic tolerance in species that experience higher climatic variability was observed in birds but not in mammals (Khaliq et al. 2014Khaliq I, Hof C, Prinzinger R, et al (2014) Global variation in thermal tolerances and vulnerability of endotherms to climate change. Proceedings of the Royal Society B: Biological Sciences 281:20141097. doi: 10.1098/rspb.2014.1097
https://doi.org/10.1098/rspb.2014.1097... ). Even though most ectotherms, particularly those from the temperate region, might tolerate projected temperature increases across significant ranges of their distributions, potential vulnerability to projected temperatures increases from polar regions to tropical areas (Khaliq et al. 2014Khaliq I, Hof C, Prinzinger R, et al (2014) Global variation in thermal tolerances and vulnerability of endotherms to climate change. Proceedings of the Royal Society B: Biological Sciences 281:20141097. doi: 10.1098/rspb.2014.1097
https://doi.org/10.1098/rspb.2014.1097... ). Unlike the observed pattern for ectotherms (Addo-Bediako et al. 2000Addo-Bediako A, Chown SL, Gaston KJ (2000) Thermal tolerance, climatic variability and latitude. Proceedings of the Royal Society B: Biological Sciences 267:739-745; Deutsch et al. 2008Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... ), endotherms present low phylogenetic conservatism regarding climatic tolerance to respond to temperature increase through physiological adaptation (Khaliq et al. 2015Khaliq I, Fritz SA, Prinzinger R, et al (2015) Global variation in thermal physiology of birds and mammals: evidence for phylogenetic niche conservatism only in the tropics. Journal of Biogeography 42:2187-2196. doi: 10.1111/jbi.12573
https://doi.org/10.1111/jbi.12573... ). In temperate regions, endotherms distribution is limited by extremes of low temperature via physiological cold tolerance of species (Khaliq et al. 2017Khaliq I, Böhning-Gaese K, Pfenninger M, et al (2017) The influence of thermal tolerances on geographical ranges of endotherms. Global Ecology and Biogeography 26:650-668. doi: 10.1111/geb.12575
https://doi.org/10.1111/geb.12575... ). Global warming scenarios might benefit species living in those regions, increasing their abundance (Carrascal et al. 2016Carrascal LM, Villén-Pérez S, Palomino D (2016) Preferred temperature and thermal breadth of birds wintering in peninsular Spain: the limited effect of temperature on species distribution. PeerJ 4:e2156. doi: 10.7717/peerj.2156
https://doi.org/10.7717/peerj.2156... ). In the tropics, endotherms (especially mammals) seem limited by other factors, such as biotic interactions, rather than climatic conditions (Khaliq et al. 2017Khaliq I, Böhning-Gaese K, Pfenninger M, et al (2017) The influence of thermal tolerances on geographical ranges of endotherms. Global Ecology and Biogeography 26:650-668. doi: 10.1111/geb.12575
https://doi.org/10.1111/geb.12575... ).

Overall, species that present the lowest climatic tolerances will be more affected by climate change. Species from the tropical region and mainly ectotherms will be more vulnerable to projected temperature increases in the future (Table 4). Endotherms can keep high and constant body temperature, which is generally independent of ambient climatic conditions (MacNab 2012McNab BK (2012) Extreme measures: the ecological energetics of birds and mammals. Chicago, IL: The University of Chicago Press). On the other hand, ectotherms might be more vulnerable as their physiology, locomotion, growth and reproduction are strongly influenced by ambient temperature (Deutsch et al. 2008Deutsch CA, Tewksbury JJ, Huey RB, et al (2008) Impacts of climate warming on terrestrial ectotherms across latitude. Proceedings of the National Academy of Sciences 105:6668-6672. doi: 10.1073/pnas.0709472105
https://doi.org/10.1073/pnas.0709472105... ). Moreover, warmer temperatures may force ectotherms to spend more time in shelters to avoid lethally high temperatures, restricting the time available for other vital activities such as foraging, territory defence and mating (Sinervo et al. 2010Sinervo B, Méndez-de-la-Cruz F, Miles DB, et al (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894-899. doi: 10.1126/science.1184695
https://doi.org/10.1126/science.1184695... ). Due to their low ability to respond to climate change, several ectotherm populations were locally extinct in recent decades, and temperature increase might lead to the extinction of almost 40% of lizard populations and 20% of lizard species globally 2080 (Sinervo et al. 2010Sinervo B, Méndez-de-la-Cruz F, Miles DB, et al (2010) Erosion of lizard diversity by climate change and altered thermal niches. Science 328:894-899. doi: 10.1126/science.1184695
https://doi.org/10.1126/science.1184695... ).

Conclusions

Overall, the literature review performed regarding the four chosen traits enabled us to present and discuss mechanisms that might explain species responses to climate change. As shown here, response to climate change is highly variable among species and regions. Some species may exhibit a critical response to a specific climate variable. In contrast, others may have a minimal response, and some might even present a contradictory response from what is expected, depending on the region they inhabit. Explaining such variation has become a significant challenge to conservationists in this century. Such explanation would allow the identification of species at higher extinction risk, the definition of the best conservation strategies, and the resources’ strategic direction. It was also possible to verify bias concerning region and taxa in the evaluated studies. The tropical region, which holds more sensitive species, was weakly represented, while most studies have focused on the temperate region. For some traits, studies concentrate on a specific group and neglect others; for example, most studies assessing climatic tolerance have concentrated on reptiles.

Species exposed to a higher magnitude of climate warming should present more pronounced biological responses (Chen et al. 2011Chen I, Hill JK, Ohlemüller R, et al (2011) Rapid range shifts of species of climate warming. Science 333:1024-1026. doi: 10.1126/science.1206432
https://doi.org/10.1126/science.1206432... ). However, intrinsic differences between species’ life-history traits, physiology and other ecological characteristics are fundamental to determine their vulnerability (Williams et al. 2008Williams SE, Shoo LP, Isaac JL, et al (2008) Towards an Integrated Framework for Assessing the Vulnerability of Species to Climate Change. PLoS Biology 6:. doi: 10.1371/journal.pbio.0060325
https://doi.org/10.1371/journal.pbio.006... ; Foden et al. 2013Foden WB, Butchart SHM, Stuart SN, et al (2013) Identifying the World’s Most Climate Change Vulnerable Species: A Systematic Trait-Based Assessment of all Birds, Amphibians and Corals. PLoS ONE 8:. doi: 10.1371/journal.pone.0065427
https://doi.org/10.1371/journal.pone.006... ). Assessments of climate change vulnerability that consider both exposure and traits that define sensitivity and adaptive ability could be helpful tools (Foden et al. 2013Foden WB, Butchart SHM, Stuart SN, et al (2013) Identifying the World’s Most Climate Change Vulnerable Species: A Systematic Trait-Based Assessment of all Birds, Amphibians and Corals. PLoS ONE 8:. doi: 10.1371/journal.pone.0065427
https://doi.org/10.1371/journal.pone.006... ; Böhm et al. 2016Böhm M, Cook D, Ma H, et al (2016) Hot and bothered: Using trait-based approaches to assess climate change vulnerability in reptiles. Biological Conservation 204:32-41. doi: 10.1016/j.biocon.2016.06.002
https://doi.org/10.1016/j.biocon.2016.06... ). However, trait choice should be based on empirical evidence that shows the relevance of such traits in determining the vulnerability of assessed species.

This review shows that the four evaluated traits are significant predictors of species responses to climate change, and we present the main mechanisms involved in each response. Therefore, clutch size, diet breadth, dispersal ability and climatic tolerance are essential traits for vulnerability assessments. Even though some evidence might lead us to conclude that species with smaller clutch size, with specialised diets, low dispersal ability and lower climatic tolerance would experience higher risk due to climate change, the set of studies evaluated here indicates that the risk depends on the region and the species group considered. While species from the temperate region could benefit from temperature increase with greater resource availability, increasing clutch size and expanding the distribution area through dispersal, species from the tropics could be severely affected. They have lower climatic tolerance and already live close to their limits of heat tolerance. Vulnerability is higher for ectotherms because, unlike endotherms, they cannot control body temperature and their biological activities depend on the climatic conditions of the environment. Ectotherms from the tropical region will not escape from temperature increase through dispersal (Buckley et al. 2013Buckley LB, Tewksbury JJ, Deutsch CA (2013) Can terrestrial ectotherms escape the heat of climate change by moving? Proceedings of the Royal Society B: Biological Sciences 280:20131149. doi: 10.1098/rspb.2013.1149
https://doi.org/10.1098/rspb.2013.1149... ).

The lack of response in a trait may interfere with the response of another feature. In the temperate region, temperature increase causes advanced flowering in plants and an abundance of insects. Thus, birds that spend the winter in other areas should advance their arrival so that the reproductive period matches food availability. Species that cannot advance their arrival might face food scarcity during reproduction, leading to smaller clutch size. In the tropics, species present lower thermic tolerance, affecting their dispersal ability to follow suitable climatic conditions if they have to cross warmer areas.

As we understand the mechanisms involved in the response of other traits, we will enhance our ability to predict climate change impacts, enabling conservation practices that are more adequate to protect species. The increase of this type of studies could facilitate understanding which characteristics are more informative to each species group within each region. Besides that, understanding the mechanisms through which traits influence species responses to climatic changes may help justify the traits included in vulnerability assessments, improving their results and making them more useful. For that, CCVAs need to be more integrated with the ecology literature to assess how species traits respond to changes in the climate.

Acknowledgements

RL research is funded by CNPq (grant #306694/2018-2). FJAB received a PhD scholarship from CNPq. This paper contributes to the INCT in Ecology, Evolution and Biodiversity Conservation founded by MCTIC/CNPq (grant #465610/2014-5) and FAPEG (grant #201810267000023). This work was supported by Brazilian Council for Scientific and Technological Development (CNPq).

References

Publication Dates

History