Which Animal Is Greatly Affected By Global Climate Change? Mec 280

i. Introduction

Anthropogenic climatic change is recognized as a major threat to global biodiversity, i that may lead to the extinction of thousands of species over the next 100 years [i–7]. Climate change is an peculiarly pernicious threat, as it may be difficult to protect species from its effects, fifty-fifty within reserves [8,9]. Furthermore, climate change may accept important interactions with other anthropogenic impacts (eastward.g. habitat loss [two,6]). Given this, understanding the responses of species to mod climate change is one of the about pressing problems facing biologists today.

But what practise we actually know about how climate change causes extinction? It might seem that limited physiological tolerances to high temperatures should be the major factor that causes climate change to threaten the persistence of populations and species, and many studies take justifiably focused on these tolerances [10–13]. Nonetheless, there may exist many other proximate causes of extinction, even when anthropogenic climate change is the ultimate cause. These proximate factors include negative impacts of heat-abstention behaviour [14], the climate-related loss of host and pollinator species [15,16] and positive impacts of climate change on pathogens and competitors [17,eighteen], among others. The relative importance of these factors is unclear and has not, to our noesis, previously been reviewed, despite increasing interest in mechanisms underlying the impacts of climate alter [19].

Identifying these proximate causes may be disquisitional for many reasons. For instance, different proximate factors may telephone call for different conservation strategies to improve their effects [20]. These dissimilar proximate factors may too influence the accuracy with which the impacts of climate change are predicted and may drive populations to extinction at different rates.

In this paper, we address three topics related to how anthropogenic climatic change causes extinction. First, nosotros briefly review and categorize the many proposed factors that potentially lead to extinction from climate change. Second, we argue that at that place is already abundant evidence for current local extinctions every bit a outcome of climatic change, based on the widespread design of range contractions at the warm edges of species' ranges (low latitude and depression elevation). Third, and most importantly, nosotros perform to the best of our cognition, the first big-scale review of empirical studies that take addressed the proximate causes of local extinctions related to climate change. This review reveals some unexpected results. We find that despite intensive research on the impacts of climate alter, only a handful of studies have demonstrated a proximate cause of local extinctions. Further, among those studies that take identified a proximate cause, very few implicate limited physiological tolerance to high temperatures as the chief, direct cause. Instead, a diverse set up of factors are supported, with species interactions beingness particularly of import. Finally, we outline some of the research approaches that can be used to examine the proximate factors causing extinction from climatic change.

2. Proximate factors causing extinction from climate change

We briefly review and categorize the various proximate factors that may crusade extinctions due to climate change. We organize these factors by distinguishing betwixt abiotic and biotic factors (following the literature on species range limits [21]). However, all factors are ultimately related to abiotic climate change.

We brand several caveats about this classification. Outset, nosotros emphasize broad categories of factors, so some specific factors may not be included. Second, some factors are soon hypothetical and have not nonetheless been demonstrated equally causes of extinction. Third, we recognize that these factors are not mutually sectional and may act synergistically to drive extinction. They may also interact with other, non-climatic factors (e.g. habitat modification [2,6]) and many different ecological and demographic factors may come into play as populations approach extinction [22]. Finally, we do not accost factors that impede climate-induced dispersal.

(a) Abiotic factors

(i) Temperature (physiological tolerances)

Many effects of anthropogenic climatic change follow from an increase in temperature. The most obvious proximate factor causing extinction is temperatures that exceed the physiological tolerance of the species [10,12]. This cistron may exist nearly important in sessile organisms and those with express thermoregulatory power, and in regions and fourth dimension scales in which temperature increase is greatest.

The impacts of temperature may also be more indirect, but still related to physiological tolerances. For example, in spiny lizards (Sceloporus), local extinctions seem to occur considering higher temperatures restrict surface activity during the spring breeding season to a daily time window that is overly brusk [23]. Similarly, increased air temperatures may both decrease activity fourth dimension and increase energy maintenance costs, leading organisms to die from starvation rather than from overheating [fourteen]. In aquatic organisms, increased water temperatures may lead to increased metabolic demand for oxygen while reducing the oxygen content of the water [24]. Variability in temperature may also be an important proximate cause of extinction [25], including both extreme events and large differences over the course of a year. In temperate and polar latitudes, a mismatch betwixt photoperiod cues and temperature may exist important, with fixed photoperiod responses leading to activity patterns that are inappropriate for the changed climate [26]. Here, both low and high temperatures could increment mortality rates and atomic number 82 to population extinction.

(ii) Precipitation (physiological tolerances)

Anthropogenic changes are also modifying precipitation patterns [27], and these changes may drive extinction in a multifariousness of ways. For example, decreasing precipitation may lead straight to h2o stress, expiry and local extinction for terrestrial species [28], and loss of habitat for freshwater species or life stages [29,xxx]. There may as well be synergistic effects between rut and drought stress (e.g. in trees [31]). Irresolute precipitation may be more of import to some species than changing temperature, sometimes leading to range shifts in the management opposite to those predicted by rising temperatures [32].

(iii) Other abiotic factors

Other abiotic, not-climatic factors may drive extinctions that are ultimately caused by climate modify. For case, climatic change can increase fire frequency, and these fires may be proximate causes of extinction (east.g. in Due south African plants [33]). Similarly, increases in temperature lead to melting icecaps and ascent body of water levels [27], which may eliminate coastal habitats and modify the salinity of freshwater habitats [34].

(b) Biotic factors

The biotic factors that are the proximate causes of extinction from climate change tin be placed in three full general categories.

(i) Negative impacts on beneficial species

Climate change may cause local extinction of a given species past causing declines in a species upon which it depends. These may include prey for predators [35], hosts for parasites and specialized herbivores [16], species that create necessary microhabitats [36] and species that are essential for reproduction (e.g. pollinators [15]).

(ii) Positive impacts on harmful species

Alternately, climatic change may crusade extinction through positive furnishings on species that accept negative interactions with a focal species, including competitors [37,38], predators [39,xl] and pathogens [41–43]. Warming temperatures tin also benefit introduced species, exacerbating their negative effects on native flora and beast [44].

(three) Temporal mismatch betwixt interacting species

Climate change may also create incongruence between the activity times of interacting species [45]. These phenological mismatches may occur when interacting species answer to unlike environmental cues (east.thou. temperature versus photoperiod for winter emergence) that are not congruently influenced by climate change [46]. We consider this category to be distinct from the other 2 considering the differences in action times are non necessarily negative or positive impacts on the species that are interacting with the focal species.

3. Are there current extinctions due to climate modify?

Our goal is to understand which proximate factors crusade extinctions due to climate alter. However, we first demand to establish that such extinctions are soon occurring. Few global species extinctions are thought to have been caused by climatic change. For example, but twenty of 864 species extinctions are considered by the International Union for Conservation of Nature (IUCN) [47] to potentially be the result of climate change, either wholly or in office (using the same search criteria as a recent review [9]), and the evidence linking them to climate alter is typically very tenuous (come across the electronic supplementary material, tabular array S1). Still, there is arable prove for local extinctions from contractions at the warm edges of species' ranges. A pattern of range shifts (generally polewards and upwards) has been documented in hundreds of species of plants and animals [48,49], and is one of the strongest signals of biotic change from global warming. These shifts effect from ii processes: cold-border expansion and warm-border wrinkle (see the electronic supplementary material, figure S1). Much has been written well-nigh common cold-edge expansions [21,50], and these may exist more common than warm-border contractions [51]. Nevertheless, many warm-edge contractions have been documented [52–58], including big-scale review studies spanning hundreds of species [48,59]. These warm-edge populations are a logical place to look for the causes of climate-related extinctions, especially because they may already exist at the limits of their climatic tolerances [60]. Importantly, this pattern of warm-edge contraction provides evidence that many local extinctions have already occurred as a upshot of climatic change.

We more often than not assume that the proximate factors causing local extinction from climate change are associated with the decease of individuals. Still, others factors may be involved too. These include emigration of individuals into adjacent localities, declines in recruitment, or a combination of these and other factors. The question of whether climate-related local extinctions occur through expiry, dispersal or other processes has received piffling attention (but run across [61,62]), and represents another important but poorly explored area in climate-modify research.

4. What causes extinction due to climate change? electric current evidence

Given that there are many different potential causes of extinction equally a result of climatic change, and given that many populations have already gone extinct (as evidenced past warm-edge range contractions), what proximate causes of climate-related extinction have actually been documented? We conducted a systematic review of the literature to accost this question.

(a) Causes of extinction: methods

Nosotros conducted three searches in the ISI Spider web of Science database, using the post-obit keywords: (i) (('locally extinct' OR 'local extinction' OR 'extinc*') AND (caus*) AND ('climate change' OR 'global warming')); (2) (('locally extinct' OR 'local extinction') AND ('climate change' OR 'global warming')); and (iii) (('extinc*' OR 'extirpat*') AND ('climate change' OR 'global warming' OR 'changing climate' OR 'global modify')). The first two were conducted on seven December 2011 and the third on 4 February 2012. Each search identified a partially overlapping set of studies (687 unique studies overall). We then reduced this to 136 studies which suggested that climate change is associated with local extinctions or declines (see the electronic supplementary material, appendix S1).

Among these 136 studies, we so identified those that reported an clan betwixt local extinction and climatic variables and that also identified a specific proximate cause for these extinctions (run into the electronic supplementary material, appendix S1). The prove linking these proximate causes to anthropogenic climate change varied considerably, but included studies integrating experimental and correlative results [23,63], and those that also accounted for factors unrelated to climate modify [64]. Although we did not perform a separate, comprehensive search for all studies of climate-related declines, we besides include studies of population declines that were connected to potential local extinctions as a second category of studies. Studies of declines should likewise be informative, given that the factors causing population declines may ultimately pb to extinctions [65]. All studies reported declines in abundance simply some as well considered declines in other parameters (e.yard. fecundity). Nosotros besides included studies of impacts from natural oscillations (such as the El Niño-Southern Oscillation, ENSO) equally a third category of results.

(b) Causes of extinction: results

(i) Proximate causes of local extinctions

Of 136 studies focusing on local extinctions associated with climate change (encounter the electronic supplementary fabric, appendix S1), only vii identified the proximate causes of these extinctions (table 1 and effigy 1a). Surprisingly, none of the vii studies shows a straightforward relationship between local extinction and express tolerances to high temperature. For case, for the two studies that relate extinctions nigh directly to changing temperatures, the proximate cistron is related either to how temperature limits surface activity time during the breeding flavour [23] or to a complex relationship between extreme temperatures (both cold and hot), precipitation and physiology [25,63]. Most studies (4 of vii) implicate species interactions every bit the proximate crusade, specially decreases in food availability [35,64,66]. Many authors have predicted that altered species interactions may be an important cause of extinction resulting from climate change (eastward.yard. [67,68]), and our results empirically support the importance of these interactions (relative to other factors) among documented cases of local extinction.

Table one. Studies documenting the proximate causes of local extinction due to anthropogenic climatic change.

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species	location	hypothesized proximate crusade of local extinction	reference
American pika (Ochotona princeps)	Neat Basin region, Us	limited tolerance to temperature extremes (both high and depression)	[25,63]
planarian (Crenobia alpina)	Wales, Uk	loss of prey equally result of increasing stream temperatures	[35]
desert bighorn sheep (Ovis canadensis)	California, U.s.a.	subtract in precipitation leading to altered plant customs (food)	[64]
checkerspot butterfly (Euphydryas editha bayensis)	San Francisco Bay area, CA, Usa	increase in variability of precipitation corresponding with reduction of temporal overlap between larvae and host plants	[66]
fish (Gobiodon sp. A)	New United kingdom of great britain and northern ireland, Papua New Guinea	destruction of obligate coral habitat due to coral bleaching caused by increasing water temperatures	[36]
48 lizard species (genus Sceloporus)	United mexican states	increased maximum air temperature approaches physiological limit, seemingly causing decreased surface activity during the reproductive season	[23]
Adrar Mountain fish species	Mauritania	loss of water bodies due to drought	[30]

Figure 1. Summary of the frequency of unlike proximate causes of extinction due to climatic change, among published studies. (a) 'local extinctions' refers to studies of local extinctions related to anthropogenic climate change (table i), (b) 'population declines' refers to studies of declines in population abundance related to anthropogenic climate alter (table 2), whereas (c) 'climatic oscillation impacts' refers to studies showing declines related to natural climatic oscillations (tabular array 3) (merely these oscillations may likewise exist influenced by human being factors, see relevant text). We note that in that location is some ambivalence in assigning some studies to a single, simple category.

(two) Proximate causes of population declines

Seven studies identified proximate causes of population declines (table 2). The frequency of different proximate causes is intriguingly similar to those for population extinctions (figure 1a,b). Specifically, species interactions are the proximate cause of declines in the majority of studies, with declines in food availability being the most common crusade [69,71,72], along with disease [70]. Drying of aquatic habitats is the cause in one study [29]. 2 studies prove physiological tolerances to abiotic factors as responsible for declines, with the declines existence due to desiccation stress in desert trees [28], and due to oxygen limitation at high temperatures in a fish [24]. However, we find again that no studies show a straightforward relationship between population declines and temperatures exceeding the critical thermal limits of physiological tolerance.

Table 2. Studies documenting the proximate causes of declines in affluence due to anthropogenic climate change.

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species	location	hypothesized proximate cause of decline	reference
aloe tree (Aloe dichotoma)	Namib desert	desiccation stress owing to decreasing precipitation	[28]
4 species of amphibians	Yellowstone National Park, USA	increasing temperature and decreasing atmospheric precipitation crusade a decline in habitat availability (pond drying)	[29]
plover (Pluvialis apricaria)	U.k.	high summertime temperatures reduce affluence of craneflies (prey)	[69]
eelpout (Zoarces viviparus)	Baltic Sea	oxygen limitation at high temperatures	[24]
frogs (genus Atelopus)	Cardinal and S America	climatic change facilitates spread of pathogen (chytrid fungus)	[70]
grey jay (Perisoreus canadensis)	Ontario, Canada	warm autumns cause rotting in hoarded food, compromising overwinter survival and breeding success in the following year	[71]
Cassin's auklet (Ptychoramphus aleuticus)	California, USA	changes in upwelling timing and forcefulness lower both adult survival and convenance success by irresolute food availability	[72]

(iii) Proximate causes of extinction due to 'natural' climatic oscillations

Among the 136 studies, iv documented proximate causes of climate-change related extinctions that were associated with climatic oscillations (table three). These oscillations may increment in frequency and severity due to anthropogenic impacts ([77], but come across [78]). All 4 studies reinforce the importance of species interactions as the proximate cause of many extinctions attributable to climatic change (figure 1c), including climate-related losses of food resources [73,75], loss of an algal symbiont ('coral bleaching'; [74]) and pathogen infection [76].

Table 3. Studies that study proximate causes of declines in abundance or fitness associated with El Niño-Southern Oscilliation (ENSO) events.

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species	location	hypothesized proximate cause of pass up	reference
fig wasps (Hymenoptera: Agonidae)	Borneo	ENSO event causes obligate host trees (Ficus sp.) to fail to produce inflorescences, resulting in local extinction of pollinating wasps	[73]
corals	Panama and Republic of ecuador	loftier sea surface temperatures cause bleaching and mortality	[74]
butterflyfish	Indian Sea	climate-related loss of coral food source	[75]
toad (Bufo boreas)	Western USA	warming reduces water depth in ponds, which increases ultraviolet-B exposure of embryos, which in turn increases risk of fungal infection	[76]

Ii of the most widely discussed examples of climate-change related extinctions involve chytrid mucus in amphibians and coral bleaching (including many examples given above [36,70,74,75]). In both cases, local extinctions are strongly connected to natural climatic oscillations (e.yard. [74]), but the links to anthropogenic climate change are all the same uncertain. For example, Pounds et al. [42] concluded that chytrid-related declines and extinctions in the frog genus Atelopus are related to anthropogenic warming, but Rohr & Raffel [70] later on suggested that chytrid spread in Atelopus was largely due to El Niño events. The link between anthropogenic climate alter and local extinction of coral populations through bleaching also remains speculative [79]. For example, severe climate anomalies can cause bleaching and coral bloodshed [80], but bleaching itself does not e'er atomic number 82 to mass bloodshed [81].

(c) Proximate causes of extinction: synthesis

Our review of the proximate causes of population extinctions and declines due to climatic change reveals three master results, which are concordant across the 3 categories of studies (extinctions, declines and climatic oscillations). First, very few studies accept documented proximate factors (eighteen of 136). Second, a diverseness of proximate causes are empirically supported. Third, irresolute interspecific interactions are the most commonly demonstrated causes of extinctions and declines (figure i). Specifically, changes in biotic interactions leading to reduced food availability are the unmarried well-nigh common proximate factor (figure one). In contrast, limited physiological tolerances to high temperatures are supported just infrequently and indirectly (figure 1). Interestingly, the impacts of species interactions may be particularly hard to document, inviting underestimation. However, we caution that these generalizations are based on few studies. For example, all three datasets (tables 1–3) are dominated by vertebrates, with only one plant study represented. Thus, the frequencies of documented proximate causes may change as the puddle of studies becomes more taxonomically representative.

Finally, we annotation that nosotros did not specifically address global species extinctions associated with climate change in our review. Nonetheless, IUCN lists 20 species equally extinct or extinct in the wild that potentially declined considering of climatic change (see the electronic supplementary cloth, table S1). Of these 20 species, seven are frogs that were peradventure infected by chytrid fungus, which may be facilitated by climate change (see higher up). 4 are snails, which may have become extinct equally a result of drought. Ii are freshwater fishes that lost their habitats because of drought. Amidst the six birds, two were also potentially affected past drought. The other 4 birds are island species possibly impacted past storms (the severity of which may exist related to climate change), only these all had clear non-climatic threats. A similar blueprint occurs in one island rodent species. In near all cases, the links between extinction and anthropogenic climate change are speculative (just see [82]), which is why these cases were non included previously in our review. Intriguingly, none of the 20 is conspicuously related to limited tolerances to loftier temperatures (see the electronic supplementary material, table S1).

5. Approaches for finding the proximate causes of climate-related extinction

Our review demonstrates that disturbingly little is known near the proximate causes of extinctions due to recent climate change. How can this important gap be filled? Many approaches are possible, and we very briefly summarize two full general frameworks that are beginning to be used. One focuses on private species at multiple localities [23,25,63], the other on species assemblages at a item locality [83–85]. These approaches are summarized graphically in the electronic supplementary cloth, figure S2.

Focusing on individual species (come across the electronic supplementary material, figure S2), one must outset certificate local extinctions or declines. To examination whether populations have gone extinct, the present and by geographical ranges of the species can be compared. These analyses need not require surveying the entire species range, merely could focus on a more limited series of transects (east.g. about the lowest latitudes and elevations, where ranges may already be limited by climatic factors [69,86]). The historical range can exist determined from literature records and/or museum specimen localities [87]. These latter data are condign increasingly bachelor through online databases (east.1000. GBIF; http://www.gbif.org/). Next, the species range (or select transects) should be resurveyed to document which populations are extant [23,56]. Evaluating whether populations persist is not trivial, and recent studies [56,88] have applied specialized approaches (east.1000. occupancy modelling [89]). Furthermore, resurveys should account for false absences that may be misinterpreted as extinctions and for biases created by unequal sampling effort in space and time [87,90,91].

Documenting climate-related declines presents different challenges than documenting extinctions, given that most species lack data on population parameters over time. Some populations have been the focus of long-term monitoring, facilitating detailed studies of climate change impacts [86,92]. Large-scale databases on population dynamics through time are now becoming bachelor. For case, the Global Population Dynamics Database [93] contains nearly 5000 fourth dimension-series datasets. However, for many species, resurveying ranges to document local extinctions may be a necessary get-go step instead.

Given demonstrable local extinctions or declines, the side by side step is to make up one's mind whether these are related to large-scale trends in global climate change. Peery et al. [94] summarize six approaches that can be used to chronicle ecology factors to population declines [95]. These aforementioned approaches can be practical to connect global climate change and local extinctions. Relationships between changes in climate over time and population extinction versus persistence can be tested using GIS-based climatic information for relatively fine time scales (e.g. each calendar month and year; PRISM; [96]). These analyses should preferably include data on other potential causes of local extinction not directly related to climate modify, such equally man habitat modification [64]. These analyses should assist establish whether the observed local extinctions or declines are indeed due to climate change. If and so, the next step is to understand their proximate causes.

Correlative analyses can be carried out to generate and exam hypotheses about which proximate causes may be involved. Biophysical modelling [97] may be especially useful for these analyses, every bit it can contain many important factors, such every bit microclimate [98] and related variables (eastward.thou. shade, current of air speed, cloudiness, humidity) and relevant behavioural, ecological, demographic and physiological parameters [14,23]. Dissecting the specific aspects of climate that are near strongly associated with local extinctions may be important (e.g. is it warmer temperatures in the hottest office of the year, or the coldest?). Correlative studies can as well exam potential biotic factors, including the clan between population extinctions or declines and the abundance of other species with negative impacts on the species in question (e.yard. competitors, pathogens) or reductions in species necessary for persistence (east.g. prey, hosts). Two-species occupancy models [99] could be practical to examination for the impacts of these and other types of interspecific interactions. Identifying the particular interactions that are responsible for climate-related extinctions may exist challenging, given the diversity of interactions and species that may be involved. Nevertheless, our results advise that changing biotic interactions may be the virtually common proximate causes of climate-related extinction (figure ane).

Once potential factors are identified with correlative studies, these can be tested with mechanistic analyses. These could include experimental tests of physiological tolerances to relevant temperature and precipitation regimes [ten,24,86,100], and laboratory and field tests of species interactions [39]. Transplant experiments that motion individuals from extant populations into nearby localities where the species has recently gone extinct [100] may exist particularly useful (for species in which this is practical). In many ways, experimental analyses tin provide the strongest tests of the hypothesized causes of local extinctions. Nevertheless, these should be informed by broader correlative studies. For example, simply testing the physiological tolerances of a species to extremely loftier temperatures may say little about the causes of climate-associated local extinction in that species if those extinctions are actually acquired past warmer temperatures in wintertime or the spread of a competitor.

The second major arroyo (come across the electronic supplementary material, figure S2) is to focus on species assemblages at single localities over time [83–85], rather than analysing multiple localities across the range of one or more species. Given data on species limerick at different points in time, the local extinctions or declines of certain species tin be tested for clan with temporal changes in climate. These losses can and then be related to specific biological traits (e.g. greater loss of species with temperature-cued flowering times versus those using photoperiod, or species for which the site is near their southern versus northern range limits [84]). These relationships can then point the fashion to more mechanistic and experimental studies.

6. Questions for future research

Understanding the proximate factors that crusade climate-related extinctions should be an urgent priority for futurity research and should open up the door to many boosted applied and basic questions. Are there specific conservation and management strategies that can be matched to specific extinction causes? Are there phylogenetic trends or life-history correlates [20] of these factors that may allow researchers to predict which factors will be of import in a species without having to conduct lengthy studies within that species? Do different factors influence the ability of niche models to accurately predict range shifts and extinctions due to climate change (east.m. physiological tolerances versus species interactions)? Tin species adapt to some potential causes of extinction and not others?

vii. Conclusions

Climatic change is now recognized as a major threat to global biodiversity, and 1 that is already causing widespread local extinctions. However, the specific causes of these present and future extinctions are much less articulate. Here, nosotros have reviewed the soon available bear witness for the proximate causes of extinction from climate change. Our review shows that only a handful of studies have focused specifically on these factors, and very few propose a straightforward human relationship between limited tolerance to loftier temperatures and local extinction. Instead, a various set of factors is implicated, including effects of precipitation, nutrient abundance and mismatched timing with host species. Overall, we fence that agreement the proximate causes of extinction from climate change should be an urgent priority for hereafter research. For example, information technology is difficult to imagine truly effective strategies for species conservation that ignore these proximate causes. We likewise outline some general approaches that may be used to identify these causes. However, nosotros brand the important caveat that the relative importance of different proximate causes may change radically over the adjacent 100 years as climate continues to alter, and limited physiological tolerances to high temperatures may become the dominant cause of extinction. Yet, our review suggests the agonizing possibility that in that location may exist many extinctions due to other proximate causes long before physiological tolerances to high temperatures become predominant.

Acknowledgements

We thank H. Resit Akçakaya, Amy Angert, Steven Beissinger, Doug Futuyma, Spencer Koury, Javier Monzón, Juan Parra and anonymous reviewers for discussion and helpful comments on the manuscript.

Footnotes

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Source: https://royalsocietypublishing.org/doi/10.1098/rspb.2012.1890

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