What Is The Relationship Between Extinction And Environmental Change

1. Introduction

Anthropogenic climate change is recognized equally a major threat to global biodiversity, one that may lead to the extinction of thousands of species over the side by side 100 years [i–7]. Climatic change is an especially pernicious threat, as it may be difficult to protect species from its furnishings, even within reserves [8,9]. Furthermore, climatic change may take of import interactions with other anthropogenic impacts (e.g. habitat loss [ii,6]). Given this, agreement the responses of species to modern climate change is one of the nigh pressing issues facing biologists today.

Merely what do we actually know about how climate alter causes extinction? It might seem that limited physiological tolerances to high temperatures should exist the major factor that causes climatic change to threaten the persistence of populations and species, and many studies have justifiably focused on these tolerances [10–13]. All the same, there may exist many other proximate causes of extinction, even when anthropogenic climatic 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 climatic change on pathogens and competitors [17,18], amidst 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 change [19].

Identifying these proximate causes may be disquisitional for many reasons. For case, unlike proximate factors may phone call for unlike conservation strategies to ameliorate their effects [twenty]. These different proximate factors may also influence the accuracy with which the impacts of climatic change are predicted and may drive populations to extinction at different rates.

In this paper, we address iii topics related to how anthropogenic climatic change causes extinction. Kickoff, we 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 testify for current local extinctions every bit a result of climate change, based on the widespread blueprint of range contractions at the warm edges of species' ranges (low latitude and low elevation). Third, and most importantly, we perform to the best of our cognition, the starting time large-calibration review of empirical studies that have addressed the proximate causes of local extinctions related to climate change. This review reveals some unexpected results. Nosotros observe that despite intensive research on the impacts of climate change, simply a scattering of studies have demonstrated a proximate cause of local extinctions. Farther, among those studies that have identified a proximate cause, very few implicate limited physiological tolerance to loftier temperatures equally the main, direct cause. Instead, a diverse set of factors are supported, with species interactions being specially important. Finally, we outline some of the research approaches that can be used to examine the proximate factors causing extinction from climate change.

2. Proximate factors causing extinction from climate modify

We briefly review and categorize the diverse proximate factors that may cause extinctions due to climate change. Nosotros organize these factors by distinguishing between 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 nearly this classification. First, we emphasize wide categories of factors, then some specific factors may not be included. 2nd, some factors are presently hypothetical and take not all the same been demonstrated as causes of extinction. Third, nosotros recognize that these factors are not mutually sectional and may act synergistically to drive extinction. They may as well interact with other, non-climatic factors (e.thousand. habitat modification [2,6]) and many different ecological and demographic factors may come up into play as populations approach extinction [22]. Finally, we do not address factors that impede climate-induced dispersal.

(a) Abiotic factors

(i) Temperature (physiological tolerances)

Many effects of anthropogenic climate modify follow from an increase in temperature. The about obvious proximate gene causing extinction is temperatures that exceed the physiological tolerance of the species [x,12]. This gene may be most important in sessile organisms and those with limited thermoregulatory ability, and in regions and time scales in which temperature increase is greatest.

The impacts of temperature may also be more than indirect, but withal related to physiological tolerances. For example, in spiny lizards (Sceloporus), local extinctions seem to occur because higher temperatures restrict surface activity during the leap breeding season to a daily time window that is overly short [23]. Similarly, increased air temperatures may both decrease activity time and increment energy maintenance costs, leading organisms to die from starvation rather than from overheating [14]. 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 big differences over the course of a year. In temperate and polar latitudes, a mismatch between photoperiod cues and temperature may be important, with fixed photoperiod responses leading to action patterns that are inappropriate for the changed climate [26]. Here, both depression and high temperatures could increase mortality rates and lead to population extinction.

(ii) Atmospheric precipitation (physiological tolerances)

Anthropogenic changes are also modifying atmospheric precipitation patterns [27], and these changes may drive extinction in a variety of ways. For instance, decreasing precipitation may atomic number 82 straight to h2o stress, death and local extinction for terrestrial species [28], and loss of habitat for freshwater species or life stages [29,thirty]. There may also be synergistic effects betwixt heat and drought stress (east.g. in copse [31]). Irresolute precipitation may be more than important 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 climatic change. For example, climate change tin can increase burn frequency, and these fires may be proximate causes of extinction (due east.one thousand. in South African plants [33]). Similarly, increases in temperature pb to melting icecaps and ascent ocean levels [27], which may eliminate coastal habitats and change the salinity of freshwater habitats [34].

(b) Biotic factors

The biotic factors that are the proximate causes of extinction from climatic change can be placed in three general categories.

(i) Negative impacts on benign species

Climate change may crusade local extinction of a given species by 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, climate change may crusade extinction through positive effects on species that have negative interactions with a focal species, including competitors [37,38], predators [39,40] and pathogens [41–43]. Warming temperatures can also do good introduced species, exacerbating their negative furnishings on native flora and animal [44].

(iii) Temporal mismatch betwixt interacting species

Climate change may too create incongruence between the activity times of interacting species [45]. These phenological mismatches may occur when interacting species respond to different environmental cues (eastward.g. temperature versus photoperiod for winter emergence) that are non congruently influenced by climatic change [46]. We consider this category to be distinct from the other two because the differences in activity 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 change?

Our goal is to empathise which proximate factors crusade extinctions due to climatic change. However, nosotros showtime demand to establish that such extinctions are presently occurring. Few global species extinctions are idea to have been caused by climate change. For instance, simply 20 of 864 species extinctions are considered by the International Spousal relationship for Conservation of Nature (IUCN) [47] to potentially be the effect of climate change, either wholly or in part (using the same search criteria as a recent review [9]), and the evidence linking them to climate alter is typically very tenuous (see the electronic supplementary material, tabular array S1). Nevertheless, in that location is abundant testify for local extinctions from contractions at the warm edges of species' ranges. A blueprint of range shifts (more often than not polewards and upward) 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 issue from two processes: cold-border expansion and warm-border contraction (see the electronic supplementary material, figure S1). Much has been written nigh cold-edge expansions [21,50], and these may be more common than warm-border contractions [51]. Nevertheless, many warm-edge contractions have been documented [52–58], including large-scale review studies spanning hundreds of species [48,59]. These warm-edge populations are a logical place to await for the causes of climate-related extinctions, especially because they may already be at the limits of their climatic tolerances [60]. Importantly, this pattern of warm-edge contraction provides bear witness that many local extinctions take already occurred as a issue of climate change.

We generally assume that the proximate factors causing local extinction from climatic change are associated with the death of individuals. Nonetheless, others factors may be involved too. These include emigration of individuals into next localities, declines in recruitment, or a combination of these and other factors. The question of whether climate-related local extinctions occur through death, dispersal or other processes has received little attending (but see [61,62]), and represents another important just poorly explored surface area in climate-change inquiry.

4. What causes extinction due to climate modify? current testify

Given that there are many different potential causes of extinction as a effect of climatic change, and given that many populations have already gone extinct (as evidenced by 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

We conducted 3 searches in the ISI 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')); (ii) (('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 7 December 2011 and the third on 4 February 2012. Each search identified a partially overlapping prepare of studies (687 unique studies overall). Nosotros 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 association between local extinction and climatic variables and that also identified a specific proximate cause for these extinctions (see the electronic supplementary material, appendix S1). The evidence linking these proximate causes to anthropogenic climatic change varied considerably, but included studies integrating experimental and correlative results [23,63], and those that also accounted for factors unrelated to climate change [64]. Although we did not perform a separate, comprehensive search for all studies of climate-related declines, we likewise include studies of population declines that were connected to potential local extinctions every bit a second category of studies. Studies of declines should also be informative, given that the factors causing population declines may ultimately lead to extinctions [65]. All studies reported declines in abundance but some also considered declines in other parameters (east.yard. fecundity). Nosotros likewise 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 (run into the electronic supplementary fabric, appendix S1), only seven identified the proximate causes of these extinctions (table 1 and figure 1a). Surprisingly, none of the seven studies shows a straightforward relationship between local extinction and limited tolerances to loftier temperature. For instance, for the two studies that relate extinctions almost directly to irresolute temperatures, the proximate factor is related either to how temperature limits surface activity time during the breeding season [23] or to a complex relationship between extreme temperatures (both cold and hot), precipitation and physiology [25,63]. Nearly studies (four of seven) implicate species interactions as the proximate cause, especially decreases in food availability [35,64,66]. Many authors have predicted that altered species interactions may be an of import cause of extinction resulting from climate modify (e.thousand. [67,68]), and our results empirically support the importance of these interactions (relative to other factors) among documented cases of local extinction.

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

Plummet

species	location	hypothesized proximate crusade of local extinction	reference
American pika (Ochotona princeps)	Corking Basin region, USA	express tolerance to temperature extremes (both high and depression)	[25,63]
planarian (Crenobia alpina)	Wales, UK	loss of prey as issue of increasing stream temperatures	[35]
desert bighorn sheep (Ovis canadensis)	California, United states	subtract in precipitation leading to altered plant customs (food)	[64]
checkerspot butterfly (Euphydryas editha bayensis)	San Francisco Bay expanse, CA, USA	increase in variability of precipitation respective with reduction of temporal overlap betwixt larvae and host plants	[66]
fish (Gobiodon sp. A)	New Britain, Papua New Guinea	devastation of obligate coral habitat due to coral bleaching acquired by increasing water temperatures	[36]
48 cadger species (genus Sceloporus)	Mexico	increased maximum air temperature approaches physiological limit, seemingly causing decreased surface activeness during the reproductive season	[23]
Adrar Mountain fish species	Mauritania	loss of water bodies due to drought	[xxx]

Figure ane. Summary of the frequency of different proximate causes of extinction due to climate change, among published studies. (a) 'local extinctions' refers to studies of local extinctions related to anthropogenic climatic change (table 1), (b) 'population declines' refers to studies of declines in population abundance related to anthropogenic climate change (table 2), whereas (c) 'climatic oscillation impacts' refers to studies showing declines related to natural climatic oscillations (table 3) (only these oscillations may also be influenced past human factors, see relevant text). Nosotros note that there is some ambiguity in assigning some studies to a single, simple category.

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(2) Proximate causes of population declines

Vii studies identified proximate causes of population declines (table ii). The frequency of unlike proximate causes is intriguingly like to those for population extinctions (effigy 1a,b). Specifically, species interactions are the proximate cause of declines in the majority of studies, with declines in food availability existence the most common cause [69,71,72], along with affliction [seventy]. Drying of aquatic habitats is the cause in i written report [29]. 2 studies show 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 observe again that no studies testify a straightforward relationship between population declines and temperatures exceeding the critical thermal limits of physiological tolerance.

Tabular array two. Studies documenting the proximate causes of declines in abundance due to anthropogenic climatic modify.

Plummet

species	location	hypothesized proximate cause of refuse	reference
aloe tree (Aloe dichotoma)	Namib desert	desiccation stress owing to decreasing precipitation	[28]
four species of amphibians	Yellowstone National Park, Usa	increasing temperature and decreasing precipitation cause a decline in habitat availability (pond drying)	[29]
plover (Pluvialis apricaria)	Britain	loftier summer temperatures reduce abundance of craneflies (prey)	[69]
eelpout (Zoarces viviparus)	Baltic Sea	oxygen limitation at high temperatures	[24]
frogs (genus Atelopus)	Central and South America	climate change facilitates spread of pathogen (chytrid fungus)	[70]
gray 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 strength lower both adult survival and convenance success past changing food availability	[72]

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

Among the 136 studies, four documented proximate causes of climate-change related extinctions that were associated with climatic oscillations (table 3). These oscillations may increase in frequency and severity due to anthropogenic impacts ([77], but run into [78]). All four studies reinforce the importance of species interactions every bit the proximate crusade of many extinctions owing to climate 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 written report proximate causes of declines in affluence or fitness associated with El Niño-Southern Oscilliation (ENSO) events.

Collapse

species	location	hypothesized proximate cause of turn down	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 Ecuador	high bounding main surface temperatures cause bleaching and mortality	[74]
butterflyfish	Indian Body of water	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]

Two of the most widely discussed examples of climate-modify related extinctions involve chytrid fungus in amphibians and coral bleaching (including many examples given in a higher place [36,70,74,75]). In both cases, local extinctions are strongly connected to natural climatic oscillations (eastward.g. [74]), just the links to anthropogenic climate alter are nevertheless uncertain. For case, Pounds et al. [42] concluded that chytrid-related declines and extinctions in the frog genus Atelopus are related to anthropogenic warming, but Rohr & Raffel [seventy] afterward 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, astringent climate anomalies tin can cause bleaching and coral mortality [lxxx], only bleaching itself does non ever pb to mass mortality [81].

(c) Proximate causes of extinction: synthesis

Our review of the proximate causes of population extinctions and declines due to climate change reveals 3 main results, which are concordant across the 3 categories of studies (extinctions, declines and climatic oscillations). Outset, very few studies have documented proximate factors (18 of 136). 2d, a diversity of proximate causes are empirically supported. Third, changing interspecific interactions are the most commonly demonstrated causes of extinctions and declines (figure ane). Specifically, changes in biotic interactions leading to reduced food availability are the unmarried most common proximate cistron (figure one). In contrast, limited physiological tolerances to high temperatures are supported only infrequently and indirectly (figure ane). Interestingly, the impacts of species interactions may be specially hard to certificate, inviting underestimation. However, nosotros circumspection that these generalizations are based on few studies. For instance, all three datasets (tables 1–three) are dominated by vertebrates, with only ane plant study represented. Thus, the frequencies of documented proximate causes may change as the pool of studies becomes more taxonomically representative.

Finally, nosotros note that we did not specifically address global species extinctions associated with climate change in our review. However, IUCN lists 20 species equally extinct or extinct in the wild that potentially declined because of climate modify (see the electronic supplementary textile, table S1). Of these 20 species, vii are frogs that were possibly infected by chytrid fungus, which may be facilitated past climate modify (see above). Four are snails, which may have go extinct as a effect of drought. Two are freshwater fishes that lost their habitats because of drought. Amongst the six birds, two were likewise potentially affected by drought. The other four birds are isle species possibly impacted past storms (the severity of which may be related to climatic change), but these all had articulate non-climatic threats. A similar pattern occurs in one island rodent species. In almost all cases, the links between extinction and anthropogenic climatic change are speculative (only run across [82]), which is why these cases were not included previously in our review. Intriguingly, none of the twenty is clearly related to express tolerances to high temperatures (run across the electronic supplementary material, tabular array S1).

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

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

Focusing on individual species (see the electronic supplementary material, figure S2), one must first document 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, but could focus on a more than limited series of transects (e.k. near the lowest latitudes and elevations, where ranges may already be express by climatic factors [69,86]). The historical range can be determined from literature records and/or museum specimen localities [87]. These latter information are becoming increasingly bachelor through online databases (e.g. 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 petty, and recent studies [56,88] have practical specialized approaches (east.g. 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 infinite and time [87,90,91].

Documenting climate-related declines presents different challenges than documenting extinctions, given that almost species lack information on population parameters over fourth dimension. Some populations accept been the focus of long-term monitoring, facilitating detailed studies of climatic change impacts [86,92]. Large-scale databases on population dynamics through fourth dimension are now becoming available. For example, the Global Population Dynamics Database [93] contains well-nigh 5000 time-serial datasets. However, for many species, resurveying ranges to document local extinctions may be a necessary beginning stride instead.

Given demonstrable local extinctions or declines, the next step is to determine whether these are related to large-scale trends in global climate change. Peery et al. [94] summarize six approaches that can exist used to relate ecology factors to population declines [95]. These aforementioned approaches can be applied 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 data for relatively fine fourth dimension scales (due east.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 alter, such as human habitat modification [64]. These analyses should help plant whether the observed local extinctions or declines are indeed due to climate change. If then, the adjacent step is to sympathise their proximate causes.

Correlative analyses tin be carried out to generate and test hypotheses well-nigh which proximate causes may exist involved. Biophysical modelling [97] may exist especially useful for these analyses, as information technology tin incorporate many of import factors, such equally microclimate [98] and related variables (e.g. shade, wind speed, cloudiness, humidity) and relevant behavioural, ecological, demographic and physiological parameters [fourteen,23]. Dissecting the specific aspects of climate that are most strongly associated with local extinctions may be important (e.yard. is it warmer temperatures in the hottest part of the year, or the coldest?). Correlative studies tin as well examination 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 (eastward.g. competitors, pathogens) or reductions in species necessary for persistence (e.g. prey, hosts). Two-species occupancy models [99] could exist practical to test 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. Even so, our results propose that changing biotic interactions may be the most common proximate causes of climate-related extinction (figure i).

One time potential factors are identified with correlative studies, these can exist 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 motility individuals from extant populations into nearby localities where the species has recently gone extinct [100] may exist peculiarly 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. However, these should exist informed by broader correlative studies. For example, simply testing the physiological tolerances of a species to extremely high temperatures may say little well-nigh the causes of climate-associated local extinction in that species if those extinctions are really acquired past warmer temperatures in winter or the spread of a competitor.

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

half dozen. Questions for futurity research

Understanding the proximate factors that cause climate-related extinctions should be an urgent priority for future research and should open the door to many additional applied and basic questions. Are there specific conservation and management strategies that tin can exist matched to specific extinction causes? Are in that location phylogenetic trends or life-history correlates [20] of these factors that may allow researchers to predict which factors volition be important in a species without having to carry 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 (eastward.g. physiological tolerances versus species interactions)? Can species adapt to some potential causes of extinction and not others?

7. Conclusions

Climate change is now recognized every bit a major threat to global biodiversity, and i that is already causing widespread local extinctions. However, the specific causes of these nowadays and futurity extinctions are much less articulate. Hither, we take 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 suggest a straightforward relationship between limited tolerance to loftier temperatures and local extinction. Instead, a diverse set of factors is implicated, including furnishings of precipitation, food affluence and mismatched timing with host species. Overall, we argue that understanding the proximate causes of extinction from climatic change should be an urgent priority for future research. For example, it 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, we make the important caveat that the relative importance of different proximate causes may change radically over the side by side 100 years equally climate continues to change, and express physiological tolerances to high temperatures may go the dominant cause of extinction. Notwithstanding, our review suggests the agonizing possibility that there may be many extinctions due to other proximate causes long earlier physiological tolerances to high temperatures go predominant.

Acknowledgements

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

Footnotes

© 2012 The Writer(s) Published by the Royal Order. All rights reserved.

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

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