How Did The Changing Climate Possibly Result In The Extinction Of These Animals?
Proc Biol Sci. 2013 Jan seven; 280(1750): 20121890.
How does climate change cause extinction?
Abigail East. Cahill,† Matthew E. Aiello-Lammens,† M. Caitlin Fisher-Reid, Xia Hua, Caitlin J. Karanewsky, Hae Yeong Ryu, Gena C. Sbeglia, Fabrizio Spagnolo, John B. Waldron, Omar Warsi, and John J. Wiens*
Received 2012 Aug xiii; Accepted 2012 Sep 24.
Abstruse
Anthropogenic climate change is predicted to be a major cause of species extinctions in the next 100 years. But what will actually cause these extinctions? For example, will it exist limited physiological tolerance to high temperatures, changing biotic interactions or other factors? Hither, we systematically review the proximate causes of climate-change related extinctions and their empirical support. We observe 136 example studies of climatic impacts that are potentially relevant to this topic. Still, only seven identified proximate causes of demonstrated local extinctions due to anthropogenic climate change. Among these 7 studies, the proximate causes vary widely. Surprisingly, none show a straightforward human relationship betwixt local extinction and limited tolerances to loftier temperature. Instead, many studies implicate species interactions as an important proximate cause, particularly decreases in food availability. We find very similar patterns in studies showing decreases in affluence associated with climate change, and in those studies showing impacts of climatic oscillations. Collectively, these results highlight our disturbingly express noesis of this crucial outcome only also back up the idea that changing species interactions are an important cause of documented population declines and extinctions related to climatic change. Finally, nosotros briefly outline general research strategies for identifying these proximate causes in time to come studies.
Keywords: climatic change, extinction, physiological tolerances, species interactions
i. Introduction
Anthropogenic climate change is recognized equally a major threat to global biodiversity, one that may pb to the extinction of thousands of species over the side by side 100 years [1–vii]. Climatic change is an peculiarly pernicious threat, every bit it may be hard to protect species from its effects, even within reserves [eight,9]. Furthermore, climate change may have important interactions with other anthropogenic impacts (e.yard. habitat loss [two,half dozen]). Given this, agreement the responses of species to modern climate change is one of the most pressing issues facing biologists today.
Merely what do we really know about how climatic change causes extinction? It might seem that limited physiological tolerances to loftier temperatures should be the major factor that causes climate change to threaten the persistence of populations and species, and many studies have justifiably focused on these tolerances [x–thirteen]. However, there may be many other proximate causes of extinction, even when anthropogenic climatic change is the ultimate cause. These proximate factors include negative impacts of oestrus-avoidance behaviour [xiv], the climate-related loss of host and pollinator species [fifteen,16] and positive impacts of climatic change on pathogens and competitors [17,18], among others. The relative importance of these factors is unclear and has not, to our noesis, previously been reviewed, despite increasing involvement in mechanisms underlying the impacts of climate modify [19].
Identifying these proximate causes may be critical for many reasons. For example, different proximate factors may call for dissimilar conservation strategies to meliorate their effects [xx]. These different proximate factors may also influence the accuracy with which the impacts of climate change are predicted and may drive populations to extinction at different rates.
In this newspaper, nosotros accost 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 there is already abundant evidence for current local extinctions as a result of climate change, based on the widespread design 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 noesis, the first large-scale review of empirical studies that have addressed the proximate causes of local extinctions related to climate modify. This review reveals some unexpected results. We notice that despite intensive research on the impacts of climatic change, merely a scattering of studies have demonstrated a proximate cause of local extinctions. Further, among those studies that have identified a proximate cause, very few implicate limited physiological tolerance to high temperatures as the main, straight cause. Instead, a various prepare of factors are supported, with species interactions being particularly of import. Finally, we outline some of the inquiry approaches that can be used to examine the proximate factors causing extinction from climate change.
2. Proximate factors causing extinction from climate change
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 make several caveats about this classification. First, we emphasize wide categories of factors, then some specific factors may non exist included. 2nd, some factors are presently hypothetical and accept not yet been demonstrated every bit causes of extinction. Third, nosotros recognize that these factors are non mutually exclusive and may act synergistically to drive extinction. They may likewise interact with other, non-climatic factors (e.1000. habitat modification [2,vi]) and many different ecological and demographic factors may come into play equally 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 change follow from an increment in temperature. The most obvious proximate cistron causing extinction is temperatures that exceed the physiological tolerance of the species [x,12]. This gene may be near 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 too exist more indirect, but still related to physiological tolerances. For example, in spiny lizards (Sceloporus), local extinctions seem to occur because college temperatures restrict surface activeness during the spring convenance season to a daily time window that is overly brusque [23]. Similarly, increased air temperatures may both subtract activity fourth dimension and increase energy maintenance costs, leading organisms to die from starvation rather than from overheating [xiv]. In aquatic organisms, increased water temperatures may pb 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 class of a yr. In temperate and polar latitudes, a mismatch betwixt photoperiod cues and temperature may be of import, with fixed photoperiod responses leading to activeness patterns that are inappropriate for the changed climate [26]. Here, both low and high temperatures could increase mortality rates and lead to population extinction.
(two) Precipitation (physiological tolerances)
Anthropogenic changes are too modifying precipitation patterns [27], and these changes may drive extinction in a multifariousness of ways. For example, decreasing precipitation may atomic number 82 directly to water stress, death and local extinction for terrestrial species [28], and loss of habitat for freshwater species or life stages [29,30]. There may also exist synergistic effects between heat and drought stress (e.g. in trees [31]). Irresolute precipitation may be more than of import to some species than changing temperature, sometimes leading to range shifts in the management opposite to those predicted past rising temperatures [32].
(three) Other abiotic factors
Other abiotic, non-climatic factors may bulldoze extinctions that are ultimately caused by climate change. For example, climate change tin can increase burn frequency, and these fires may be proximate causes of extinction (due east.g. in South African plants [33]). Similarly, increases in temperature lead to melting icecaps and rising bounding main levels [27], which may eliminate coastal habitats and alter the salinity of freshwater habitats [34].
(b) Biotic factors
The biotic factors that are the proximate causes of extinction from climate change can be placed in three general categories.
(i) Negative impacts on beneficial species
Climate change may crusade local extinction of a given species by causing declines in a species upon which information technology depends. These may include prey for predators [35], hosts for parasites and specialized herbivores [xvi], 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 cause extinction through positive effects on species that take negative interactions with a focal species, including competitors [37,38], predators [39,40] and pathogens [41–43]. Warming temperatures can too benefit introduced species, exacerbating their negative effects on native flora and fauna [44].
(three) Temporal mismatch between interacting species
Climate change may too create incongruence between the activity times of interacting species [45]. These phenological mismatches may occur when interacting species reply to dissimilar environmental cues (due east.1000. temperature versus photoperiod for winter emergence) that are not congruently influenced past climate alter [46]. Nosotros consider this category to be distinct from the other two because 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 change?
Our goal is to empathise which proximate factors cause extinctions due to climate change. However, we offset need to establish that such extinctions are presently occurring. Few global species extinctions are thought to have been caused past climatic change. For case, only 20 of 864 species extinctions are considered by the International Union for Conservation of Nature (IUCN) [47] to potentially exist the result of climate change, either wholly or in office (using the same search criteria as a contempo review [nine]), and the evidence linking them to climate change is typically very tenuous (see the electronic supplementary material, table S1). All the same, there is abundant evidence 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 ane of the strongest signals of biotic change from global warming. These shifts issue from two processes: common cold-edge expansion and warm-border contraction (meet the electronic supplementary textile, figure S1). Much has been written about cold-border expansions [21,50], and these may be more than common than warm-border contractions [51]. Nonetheless, many warm-edge contractions accept been documented [52–58], including large-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 take already occurred equally a result of climate alter.
We generally assume that the proximate factors causing local extinction from climatic change are associated with the death of individuals. However, 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 research.
4. What causes extinction due to climate change? current testify
Given that there are many different potential causes of extinction as a issue of climate change, and given that many populations have already gone extinct (as evidenced by warm-border range contractions), what proximate causes of climate-related extinction take actually been documented? Nosotros conducted a systematic review of the literature to accost this question.
(a) Causes of extinction: methods
We conducted three searches in the ISI Web of Science database, using the following keywords: (i) (('locally extinct' OR 'local extinction' OR 'extinc*') AND (caus*) AND ('climate modify' 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 change')). The get-go 2 were conducted on 7 December 2011 and the 3rd on four 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 modify is associated with local extinctions or declines (meet the electronic supplementary material, appendix S1).
Among these 136 studies, we then identified those that reported an clan between 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 evidence 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 change [64]. Although nosotros did not perform a separate, comprehensive search for all studies of climate-related declines, we also include studies of population declines that were connected to potential local extinctions as a 2d category of studies. Studies of declines should also exist 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 (due east.g. fecundity). We also included studies of impacts from natural oscillations (such as the El Niño-Southern Oscillation, ENSO) as 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 (see the electronic supplementary fabric, appendix S1), only seven identified the proximate causes of these extinctions (table 1 and figure 1 a). Surprisingly, none of the seven studies shows a straightforward human relationship between local extinction and express tolerances to loftier temperature. For case, for the ii studies that relate extinctions most directly to irresolute temperatures, the proximate factor is related either to how temperature limits surface activity fourth dimension during the breeding season [23] or to a circuitous relationship between farthermost 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 nutrient availability [35,64,66]. Many authors have predicted that altered species interactions may be an important crusade of extinction resulting from climate change (east.g. [67,68]), and our results empirically support the importance of these interactions (relative to other factors) among documented cases of local extinction.
Tabular array 1.
Studies documenting the proximate causes of local extinction due to anthropogenic climatic change.
| species | location | hypothesized proximate cause of local extinction | reference |
|---|---|---|---|
| American pika (Ochotona princeps) | Corking Basin region, U.s.a. | limited tolerance to temperature extremes (both high and depression) | [25,63] |
| planarian (Crenobia alpina) | Wales, Great britain | loss of prey equally upshot of increasing stream temperatures | [35] |
| desert bighorn sheep (Ovis canadensis) | California, United states of america | subtract in precipitation leading to altered plant community (nutrient) | [64] |
| checkerspot butterfly (Euphydryas editha bayensis) | San Francisco Bay area, CA, Usa | increase in variability of atmospheric precipitation corresponding with reduction of temporal overlap betwixt larvae and host plants | [66] |
| fish (Gobiodon sp. A) | New Britain, Papua New Guinea | destruction of obligate coral habitat due to coral bleaching acquired past increasing water temperatures | [36] |
| 48 lizard species (genus Sceloporus) | Mexico | increased maximum air temperature approaches physiological limit, seemingly causing decreased surface action during the reproductive season | [23] |
| Adrar Mountain fish species | Islamic republic of mauritania | loss of water bodies due to drought | [30] |
Summary of the frequency of unlike proximate causes of extinction due to climate change, among published studies. (a) 'local extinctions' refers to studies of local extinctions related to anthropogenic climate modify (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 iii) (simply these oscillations may also be influenced by homo factors, see relevant text). We annotation that there is some ambiguity in assigning some studies to a single, unproblematic category.
(2) Proximate causes of population declines
Seven studies identified proximate causes of population declines (table two). The frequency of different proximate causes is intriguingly similar to those for population extinctions (figure ane a,b). Specifically, species interactions are the proximate cause of declines in the majority of studies, with declines in nutrient availability being the almost common crusade [69,71,72], along with disease [seventy]. Drying of aquatic habitats is the cause in i study [29]. Two studies show physiological tolerances to abiotic factors as responsible for declines, with the declines being due to desiccation stress in desert copse [28], and due to oxygen limitation at loftier temperatures in a fish [24]. Withal, nosotros discover again that no studies testify a straightforward relationship betwixt population declines and temperatures exceeding the critical thermal limits of physiological tolerance.
Table 2.
Studies documenting the proximate causes of declines in abundance due to anthropogenic climate change.
| species | location | hypothesized proximate cause of turn down | reference |
|---|---|---|---|
| aloe tree (Aloe dichotoma) | Namib desert | desiccation stress attributable to decreasing precipitation | [28] |
| four species of amphibians | Yellowstone National Park, Usa | increasing temperature and decreasing precipitation crusade a decline in habitat availability (pond drying) | [29] |
| plover (Pluvialis apricaria) | United Kingdom | loftier summer temperatures reduce abundance of craneflies (prey) | [69] |
| eelpout (Zoarces viviparus) | Baltic Body of water | oxygen limitation at loftier temperatures | [24] |
| frogs (genus Atelopus) | Key and South America | climate 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 post-obit year | [71] |
| Cassin's auklet (Ptychoramphus aleuticus) | California, Us | changes in upwelling timing and strength lower both developed survival and convenance success past changing food availability | [72] |
(three) Proximate causes of extinction due to 'natural' climatic oscillations
Among the 136 studies, 4 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 iv studies reinforce the importance of species interactions as the proximate cause of many extinctions attributable to climate modify (effigy i c), including climate-related losses of food resources [73,75], loss of an algal symbiont ('coral bleaching'; [74]) and pathogen infection [76].
Tabular array three.
Studies that study proximate causes of declines in abundance or fitness associated with El Niño-Southern Oscilliation (ENSO) events.
| species | location | hypothesized proximate cause of reject | 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 ocean surface temperatures crusade bleaching and mortality | [74] |
| butterflyfish | Indian Ocean | climate-related loss of coral nutrient source | [75] |
| toad (Bufo boreas) | Western United states | warming reduces water depth in ponds, which increases ultraviolet-B exposure of embryos, which in turn increases risk of fungal infection | [76] |
2 of the almost widely discussed examples of climate-change related extinctions involve chytrid mucus in amphibians and coral bleaching (including many examples given above [36,seventy,74,75]). In both cases, local extinctions are strongly connected to natural climatic oscillations (eastward.k. [74]), but the links to anthropogenic climate change are still uncertain. For example, Pounds et al. [42] ended that chytrid-related declines and extinctions in the frog genus Atelopus are related to anthropogenic warming, but Rohr & Raffel [70] afterwards suggested that chytrid spread in Atelopus was largely due to El Niño events. The link between anthropogenic climatic change and local extinction of coral populations through bleaching too remains speculative [79]. For instance, severe climate anomalies can cause bleaching and coral bloodshed [80], merely bleaching itself does not always lead to mass mortality [81].
(c) Proximate causes of extinction: synthesis
Our review of the proximate causes of population extinctions and declines due to climatic change reveals three principal results, which are concordant beyond the 3 categories of studies (extinctions, declines and climatic oscillations). Kickoff, very few studies accept documented proximate factors (eighteen of 136). Second, a diverseness of proximate causes are empirically supported. Third, changing interspecific interactions are the nearly commonly demonstrated causes of extinctions and declines (effigy one). Specifically, changes in biotic interactions leading to reduced food availability are the single nigh common proximate factor (figure one). In contrast, limited physiological tolerances to loftier temperatures are supported only infrequently and indirectly (figure 1). Interestingly, the impacts of species interactions may be peculiarly difficult to certificate, inviting underestimation. However, we circumspection that these generalizations are based on few studies. For case, all three datasets (tables 1–3) are dominated by vertebrates, with only one found written report represented. Thus, the frequencies of documented proximate causes may change equally the pool of studies becomes more taxonomically representative.
Finally, we note that we did not specifically address global species extinctions associated with climate change in our review. Withal, IUCN lists xx species as extinct or extinct in the wild that potentially declined because of climate change (run across the electronic supplementary material, tabular array S1). Of these 20 species, seven are frogs that were mayhap infected by chytrid fungus, which may be facilitated by climate modify (run into above). Iv are snails, which may take go extinct as a outcome of drought. 2 are freshwater fishes that lost their habitats considering of drought. Amid the six birds, ii were also potentially affected by drought. The other four birds are island species possibly impacted past storms (the severity of which may be related to climate change), only these all had clear non-climatic threats. A similar pattern occurs in one island rodent species. In virtually all cases, the links between extinction and anthropogenic climate alter are speculative (but see [82]), which is why these cases were not included previously in our review. Intriguingly, none of the xx is clearly related to express tolerances to high temperatures (encounter the electronic supplementary material, table S1).
v. Approaches for finding the proximate causes of climate-related extinction
Our review demonstrates that disturbingly little is known about the proximate causes of extinctions due to recent climate change. How can this of import gap exist filled? Many approaches are possible, and nosotros very briefly summarize two 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 particular locality [83–85]. These approaches are summarized graphically in the electronic supplementary fabric, figure S2.
Focusing on individual species (see the electronic supplementary material, effigy S2), 1 must commencement document local extinctions or declines. To exam whether populations have gone extinct, the present and past geographical ranges of the species tin can be compared. These analyses demand not require surveying the entire species range, simply could focus on a more limited serial of transects (e.g. nigh the lowest latitudes and elevations, where ranges may already be limited by climatic factors [69,86]). The historical range can be determined from literature records and/or museum specimen localities [87]. These latter data are becoming increasingly available through online databases (e.chiliad. 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 applied specialized approaches (due east.g. occupancy modelling [89]). Furthermore, resurveys should business relationship for false absences that may be misinterpreted as extinctions and for biases created by unequal sampling endeavor in infinite and time [87,90,91].
Documenting climate-related declines presents different challenges than documenting extinctions, given that almost 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-calibration databases on population dynamics through time are now condign available. For example, the Global Population Dynamics Database [93] contains virtually 5000 fourth dimension-series datasets. However, for many species, resurveying ranges to document local extinctions may be a necessary first stride instead.
Given demonstrable local extinctions or declines, the next pace is to decide whether these are related to big-calibration trends in global climate alter. Peery et al. [94] summarize six approaches that can be used to relate environmental factors to population declines [95]. These same approaches tin be applied to connect global climate change and local extinctions. Relationships between changes in climate over fourth dimension and population extinction versus persistence can be tested using GIS-based climatic data for relatively fine time scales (e.g. each month and twelvemonth; PRISM; [96]). These analyses should preferably include data on other potential causes of local extinction not straight related to climate change, such every bit human habitat modification [64]. These analyses should help institute whether the observed local extinctions or declines are indeed due to climate change. If so, the next footstep is to understand their proximate causes.
Correlative analyses tin can be carried out to generate and exam hypotheses well-nigh which proximate causes may be involved. Biophysical modelling [97] may exist especially useful for these analyses, as information technology can incorporate many important factors, such as microclimate [98] and related variables (e.g. 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 about strongly associated with local extinctions may exist important (e.g. is it warmer temperatures in the hottest part of the year, or the coldest?). Correlative studies can also test potential biotic factors, including the association between population extinctions or declines and the abundance of other species with negative impacts on the species in question (e.g. competitors, pathogens) or reductions in species necessary for persistence (e.g. prey, hosts). Ii-species occupancy models [99] could be applied 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 be challenging, given the diversity of interactions and species that may be involved. However, our results advise that changing biotic interactions may be the almost common proximate causes of climate-related extinction (figure one).
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 [10,24,86,100], and laboratory and field tests of species interactions [39]. Transplant experiments that move individuals from extant populations into nearby localities where the species has recently gone extinct [100] may be specially useful (for species in which this is practical). In many means, experimental analyses tin can provide the strongest tests of the hypothesized causes of local extinctions. Yet, these should exist informed past broader correlative studies. For example, only 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 really caused past warmer temperatures in winter or the spread of a competitor.
The second major arroyo (run into the electronic supplementary material, figure S2) is to focus on species assemblages at unmarried localities over fourth dimension [83–85], rather than analysing multiple localities across the range of 1 or more species. Given information on species composition at unlike points in time, the local extinctions or declines of certain species can be tested for clan with temporal changes in climate. These losses can then be related to specific biological traits (east.1000. greater loss of species with temperature-cued flowering times versus those using photoperiod, or species for which the site is well-nigh 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
Agreement the proximate factors that cause climate-related extinctions should be an urgent priority for hereafter research and should open the door to many additional practical and basic questions. Are there specific conservation and management strategies that can exist matched to specific extinction causes? Are there phylogenetic trends or life-history correlates [xx] of these factors that may allow researchers to predict which factors volition be important in a species without having to deport lengthy studies within that species? Exercise different factors influence the ability of niche models to accurately predict range shifts and extinctions due to climate alter (e.k. physiological tolerances versus species interactions)? Can species adapt to some potential causes of extinction and not others?
7. Conclusions
Climatic change is now recognized every bit 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 clear. Hither, we have reviewed the presently available evidence for the proximate causes of extinction from climatic 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 various set of factors is implicated, including effects of precipitation, nutrient affluence and mismatched timing with host species. Overall, we argue that understanding the proximate causes of extinction from climate change should be an urgent priority for hereafter inquiry. For example, information technology is difficult to imagine truly effective strategies for species conservation that ignore these proximate causes. We as well outline some general approaches that may be used to identify these causes. Notwithstanding, we make the important caveat that the relative importance of different proximate causes may modify radically over the next 100 years as climate continues to change, and limited physiological tolerances to high temperatures may go the dominant cause of extinction. Nevertheless, our review suggests the disturbing possibility that there may exist many extinctions due to other proximate causes long before physiological tolerances to loftier temperatures become predominant.
Acknowledgements
We give thanks H. Resit Akçakaya, Amy Angert, Steven Beissinger, Doug Futuyma, Spencer Koury, Javier Monzón, Juan Parra and anonymous reviewers for word and helpful comments on the manuscript.
References
3. Leadley P., et al. Biodiversity scenarios: projections of 21st century alter in biodiversity and associated ecosystem services. 2010. Secretariat of the Convention on Biological Diversity, Montreal, 2010.
5. Dawson T. P., Jackson South. T., House J. I., Prentice I. C., Mace G. Thou. 2011. Beyond predictions: biodiversity conservation in a changing climate. Scientific discipline 332, 53–58 10.1126/scientific discipline.1200303 (doi:10.1126/science.1200303) [PubMed] [CrossRef] [Google Scholar]
6. Hof C., Araujo M. B., Jetz West., Rahbek C. 2011. Condiment threats from pathogens, climate and land-use alter for global amphibian diversity. Nature 480, 516–519 10.1038/nature10650 (doi:10.1038/nature10650) [PubMed] [CrossRef] [Google Scholar]
8. Loarie S. R., Duffy P. B., Hamilton H., Asner G. P., Field C. B., Ackerly D. D. 2009. The velocity of climatic change. Nature 462, 1052–1055 10.1038/nature08649 (doi:10.1038/nature08649) [PubMed] [CrossRef] [Google Scholar]
ix. Monzón J., Moyer-Horner L., Palamar M. B. 2011. Climate change and species range dynamics in protected areas. BioScience 61, 752–761 10.1525/bio.2011.61.x.five (doi:10.1525/bio.2011.61.10.five) [CrossRef] [Google Scholar]
ten. Deutsch C. A., Tewksbury J. J., Huey R. B., Sheldon Thou. Southward., Ghalambor C. M., Haak D. C., Martin P. R. 2008. Impacts of climate warming on terrestrial ectotherms across latitude. Proc. Natl Acad. Sci. USA 105, 6668–6672 10.1073/pnas.0709472105 (doi:10.1073/pnas.0709472105) [PMC costless article] [PubMed] [CrossRef] [Google Scholar]
eleven. Huey R. B., Deutsch C. A., Tewksbury J. J., Vitt L. J., Hertz P. Eastward., Perez H. J. A., Garland T. 2009. Why tropical forest lizards are vulnerable to climate warming. Proc. R. Soc. B 276, 1939–1948 10.1098/rspb.2008.1957 (doi:10.1098/rspb.2008.1957) [PMC gratuitous commodity] [PubMed] [CrossRef] [Google Scholar]
12. Somero G. N. 2010. The physiology of climate modify: how potentials for acclimatization and genetic accommodation will determine 'winners' and 'losers'. J. Exp. Biol. 213, 912–920 10.1242/jeb.037473 (doi:10.1242/jeb.037473) [PubMed] [CrossRef] [Google Scholar]
13. Somero G. N. 2011. Comparative physiology: a 'crystal ball' for predicting consequences of global change. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301, R1–R14 10.1152/ajpregu.00719.2010 (doi:x.1152/ajpregu.00719.2010) [PubMed] [CrossRef] [Google Scholar]
fourteen. Kearney M., Shine R., Porter W. P. 2009. The potential for behavioral thermoregulation to buffer 'cold-blooded' animals confronting climate warming. Proc. Natl Acad. Sci. The states 106, 3835–3840 10.1073/pnas.0808913106 (doi:10.1073/pnas.0808913106) [PMC free article] [PubMed] [CrossRef] [Google Scholar]
sixteen. Schweiger O., Heikkinen R.K., Harpke A., Hickler T., Klotz S., Kudrna O., Kühn I., Pöyry J., Settele J. 2012. Increasing range mismatching of interacting species under global change is related to their ecological characteristics. Glob. Ecol. Biogeogr. 21, 88–99 x.1111/j.1466-8238.2010.00607.x (doi:ten.1111/j.1466-8238.2010.00607.x) [CrossRef] [Google Scholar]
17. Tylianakis J. M., Didham R. K., Bascompte J., Wardle D. A. 2008. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. eleven, 1351–1363 x.1111/j.1461-0248.2008.01250.x (doi:10.1111/j.1461-0248.2008.01250.10) [PubMed] [CrossRef] [Google Scholar]
eighteen. Bonelli Southward., Cerrato C., Loglisci N., Balletto E. 2011. Population extinctions in the Italian diurnal Lepidoptera: an analysis of possible causes. J. Insect Conserv. 15, 879–890 10.1007/s10841-011-9387-6 (doi:10.1007/s10841-011-9387-six) [CrossRef] [Google Scholar]
nineteen. Beever J. A., Belant J. Fifty. (eds) 2012. Ecological consequences of climate modify. Mechanisms, conservation, and management. Boca Raton, FL: CRC Press [Google Scholar]
20. Beever J. A., Belant J. 50. 2012. Ecological consequences of climatic change: synthesis and enquiry needs. In Ecological consequences of climatic change. Mechanisms, conservation, and management (eds Beever J. A., Belant J. L.), pp. 285–294 Boca Raton, FL: CRC Press [Google Scholar]
21. Sexton J. P., McIntyre P. J., Angert A. L., Rice M. J. 2009. Evolution and ecology of species range limits. Annu. Rev. Ecol. Evol. Syst. 40, 415–436 10.1146/annurev.ecolsys.110308.120317 (doi:10.1146/annurev.ecolsys.110308.120317) [CrossRef] [Google Scholar]
22. Brook B. W., Sodhi N.S., Bradshaw C. J. A. 2008. Synergies amidst extinction risks nether global modify. Trends Ecol. Evol. 23, 453–460 ten.1016/j.tree.2008.03.011 (doi:ten.1016/j.tree.2008.03.011) [PubMed] [CrossRef] [Google Scholar]
24. Pörtner H. O., Knust R. 2007. Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315, 95–97 10.1126/science.1135471 (doi:ten.1126/science.1135471) [PubMed] [CrossRef] [Google Scholar]
25. Beever E. A., Ray C., Wilkening J. L., Brussard P. F., Mote P. W. 2011. Contemporary climate change alters the pace and drivers of extinction. Glob. Change Biol. 17, 2054–2070 10.1111/j.1365-2486.2010.02389.x (doi:10.1111/j.1365-2486.2010.02389.x) [CrossRef] [Google Scholar]
26. Bradshaw W. E., Holzapfel C. Grand. 2010. Light, time, and the physiology of biotic response to rapid climate change in animals. Annu. Rev. Physiol. 72, 147–166 10.1146/annurev-physiol-021909-135837 (doi:10.1146/annurev-physiol-021909-135837) [PubMed] [CrossRef] [Google Scholar]
27. IPCC 2007. Climate change 2007, synthesis report. In Contributions of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climage Change (eds Cadre Writing Team, Pachauri R. Grand., Reisinger A.), pp. 104 Geneva, Switzerland: IPCC [Google Scholar]
28. Foden West., et al. 2007. A changing climate is eroding the geographical range of the Namib Desert tree aloe through population declines and dispersal lags. Divers. Distrib. 13, 645–653 10.1111/j.1472-4642.2007.00391.x (doi:10.1111/j.1472-4642.2007.00391.x) [CrossRef] [Google Scholar]
29. McMenamin S. 1000., Hadley East. A., Wright C. One thousand. 2008. Climatic modify and wetland desiccation cause amphibian decline in Yellowstone National Park. Proc. Natl Acad. Sci. USA 105, 16 988–16 993 10.1073/pnas.0809090105 (doi:x.1073/pnas.0809090105) [PMC free commodity] [PubMed] [CrossRef] [Google Scholar]
31. Adams H. D., Guardiola-Claramonte K., Barron-Gafford 1000. A., Villegas J. C., Breshears D. D., Zou C. B., Troch P. A., Huxman T. E. 2009. Temperature sensitivity of drought-induced tree mortality portends increased regional die-off under global modify-type drought. Proc. Natl Acad. Sci. United states of america 106, 7063–7066 10.1073/pnas.0901438106 (doi:10.1073/pnas.0901438106) [PMC free commodity] [PubMed] [CrossRef] [Google Scholar]
32. Crimmins Southward. M., Dobrowski S. Z., Greenberg J. A., Abatzoglou J. T., Mynsberge A. R. 2011. Changes in climatic water balance drive downhill shifts in plant species' optimum elevations. Science 331, 324–327 10.1126/science.1199040 (doi:x.1126/science.1199040) [PubMed] [CrossRef] [Google Scholar]
33. Keith D. A., Akçakaya H. R., Thuiller Westward., Midgley K. F., Pearson R. Thousand., Phillips S. J., Regan H. Thou., Araújo One thousand. B., Rebelo T. G. 2008. Predicting extinction risks nether climate modify: coupling stochastic population models with dynamic bioclimatic habitat models. Biol. Lett. 4, 560–563 x.1098/rsbl.2008.0049 (doi:10.1098/rsbl.2008.0049) [PMC costless article] [PubMed] [CrossRef] [Google Scholar]
34. Jones A. R. 2012. Climate change and sandy beach ecosystems. In Ecological consequences of climate change. Mechanisms, conservation, and management (eds Beever J. A., Belant J. Fifty.), pp. 133–159 Boca Raton, FL: CRC Press [Google Scholar]
35. Durance I., Ormerod S. J. 2010. Evidence for the role of climate in the local extinction of a absurd-water triclad. J. N. Am. Benthol. Soc. 29, 1367–1378 10.1899/09-159.1 (doi:10.1899/09-159.1) [CrossRef] [Google Scholar]
37. Wethey D. S. 2002. Biogeography, competition, and microclimate: the barnacle Chthamalus fragilis in New England. Integr. Comp. Biol. 42, 872–880 ten.1093/icb/42.4.872 (doi:10.1093/icb/42.4.872) [PubMed] [CrossRef] [Google Scholar]
38. Suttle K. B., Thomsen Yard. A., Power One thousand. E. 2007. Species interactions reverse grassland responses to changing climate. Science 315, 640–642 ten.1126/science.1136401 (doi:ten.1126/science.1136401) [PubMed] [CrossRef] [Google Scholar]
39. Goddard J. H. R., Gosliner T. Thousand., Pearse J. S. 2011. Impacts associated with the recent range shift of the aeolid nudibranch Phidiana hiltoni (Mollusca, Opisthobranchia) in California. Mar. Biol. 158, 1095–1109 10.1007/s00227-011-1633-7 (doi:10.1007/s00227-011-1633-7) [PMC free article] [PubMed] [CrossRef] [Google Scholar]
41. Benning T. 50., LaPointe D., Atkinson C. T., Vitousek P. M. 2002. Interactions of climatic change with biological invasions and state apply in the Hawaiian Islands: modeling the fate of endemic birds using a geographic information arrangement. Proc. Natl Acad. Sci. USA 99, xiv 246–14 249 x.1073/pnas.162372399 (doi:ten.1073/pnas.162372399) [PMC complimentary article] [PubMed] [CrossRef] [Google Scholar]
42. Pounds J. A., et al. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439, 161–167 10.1038/nature04246 (doi:10.1038/nature04246) [PubMed] [CrossRef] [Google Scholar]
43. Ytrehus B., Bretten T., Bergsjø B., Isaksen K. 2008. Fatal pneumonia epizootic in musk ox (Ovibos moschatus) in a menstruation of extraordinary atmospheric condition conditions. Ecohealth 5, 213–223 10.1007/s10393-008-0166-0 (doi:10.1007/s10393-008-0166-0) [PubMed] [CrossRef] [Google Scholar]
44. Stachowicz J. J., Terwin J. R., Whitlach R. B., Osman R. Due west. 2002. Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc. Natl Acad. Sci. USA 99, fifteen 497–15 500 ten.1073/pnas.242437499 (doi:ten.1073/pnas.242437499) [PMC free commodity] [PubMed] [CrossRef] [Google Scholar]
45. Visser M. Eastward., van Noordwijk A. J., Tinbergen J. Thou., Lessells C. M. 1998. Warmer springs lead to mistimed reproduction in great tits (Parus major). Proc. R. Soc. Lond. B 265, 1867–1870 ten.1098/rspb.1998.0514 (doi:10.1098/rspb.1998.0514) [CrossRef] [Google Scholar]
48. Parmesan C., Yohe G. 2003. A globally coherent fingerprint of climatic change impacts across natural systems. Nature 421, 37–42 10.1038/nature01286 (doi:10.1038/nature01286) [PubMed] [CrossRef] [Google Scholar]
fifty. Angert A. Fifty., Crozier 50. One thousand., Rissler L. J., Gilman S. E., Tewksbury J. J., Chunco A. J. 2011. Practise species' traits predict recent shifts at expanding range edges? Ecol. Lett. fourteen, 677–689 ten.1111/j.1461-0248.2011.01620.x (doi:x.1111/j.1461-0248.2011.01620.x) [PubMed] [CrossRef] [Google Scholar]
51. Parmesan C., Gaines S., Gonzalez 50., Kaufman D. M., Kingsolver J., Peterson A. T., Sagarin R. 2005. Empirical perspectives on species borders: from traditional biogeography to global change. Oikos 108, 58–75 x.1111/j.0030-1299.2005.13150.10 (doi:10.1111/j.0030-1299.2005.13150.x) [CrossRef] [Google Scholar]
52. Hickling R., Roy D. B., Hill J. G., Thomas C. D. 2005. A n shift of range margins in the British Odonata. Glob. Change Biol. xi, 502–506 10.1111/j.1365-2486.2005.00904.ten (doi:x.1111/j.1365-2486.2005.00904.ten) [CrossRef] [Google Scholar]
53. Perry A. L., Low P. J., Ellis J. R., Reynolds J. D. 2005. Climate change and distribution shifts in marine species. Science 308, 1912–1915 10.1126/scientific discipline.1111322 (doi:ten.1126/scientific discipline.1111322) [PubMed] [CrossRef] [Google Scholar]
54. Wilson J. West., Gutierrez D., Martinez D., Agudo R., Monserrat V. J. 2005. Changes to the elevational limits and extent of species ranges associated with climate modify. Ecol. Lett. 8, 1138–1146 10.1111/j.1461-0248.2005.00824.ten (doi:10.1111/j.1461-0248.2005.00824.x) [PubMed] [CrossRef] [Google Scholar]
55. Thomas C. D., Franco A. Yard. A., Hill J. Thousand. 2006. Range retractions and extinctions in the confront of climate warming. Trends Ecol. Evol. 21, 415–416 x.1016/j.tree.2006.05.012 (doi:10.1016/j.tree.2006.05.012) [PubMed] [CrossRef] [Google Scholar]
56. Moritz C., Patton J. L., Conroy C. J., Parra J. L., White Chiliad. C., Beissinger South. R. 2008. Bear upon of a century of climate change on modest-mammal communities in Yosemite National Park, USA. Science 322, 261–264 10.1126/science.1163428 (doi:10.1126/science.1163428) [PubMed] [CrossRef] [Google Scholar]
57. Hawkins S. J., et al. 2009. Consequences of climate-driven biodiversity changes for ecosystem functioning of North European rocky shores. Mar. Ecol. Prog. Ser. 396, 245–259 10.3354/meps08378 (doi:10.3354/meps08378) [CrossRef] [Google Scholar]
58. Jones South. J., Lima F. P., Wethey D. Southward. 2010. Ascent ecology temperatures and biogeography: poleward range contraction of the bluish mussel, Mytilus edulis 50., in the western Atlantic. J. Biogeogr. 37, 2243–2259 x.1111/j.1365-2699.2010.02386.ten (doi:10.1111/j.1365-2699.2010.02386.10) [CrossRef] [Google Scholar]
59. Chen I. C., Hill J. K., Ohlemuller R., Roy D. B., Thomas C. D. 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 10.1126/scientific discipline.1206432 (doi:ten.1126/scientific discipline.1206432) [PubMed] [CrossRef] [Google Scholar]
threescore. Anderson B. J., Akçakaya H. R., Araújo M. B., Fordham D. A., Martinez-Meyer E., Thuiller W., Beck B. W. 2009. Dynamics of range margins for metapopulations nether climatic change. Proc. R. Soc. B 276, 1415–1420 10.1098/rspb.2008.1681 (doi:x.1098/rspb.2008.1681) [PMC free article] [PubMed] [CrossRef] [Google Scholar]
61. Gilchrist H. Thou., Mallory M. L. 2005. Declines in affluence and distribution of the ivory gull (Pagophila eburnea) in Arctic Canada. Biol. Conserv. 121, 303–309 10.1016/j.biocon.2004.04.021 (doi:10.1016/j.biocon.2004.04.021) [CrossRef] [Google Scholar]
62. Tyler N. J. C. 2010. Climate, snowfall, ice, crashes, and declines in populations of reindeer and caribou (Rangifer tarandus 50.). Ecol. Monogr. eighty, 197–219 10.1890/09-1070.one (doi:10.1890/09-1070.1) [CrossRef] [Google Scholar]
63. Beever E. A., Ray C., Mote P. Westward., Wilkening J. L. 2010. Testing alternative models of climate-mediated extirpations. Conserv. Biol. 20, 164–178 x.1890/08-1011.i (doi:10.1890/08-1011.1) [PubMed] [CrossRef] [Google Scholar]
64. Epps C. Due west., McCullough D., Wehausen J. D., Bleich V. C., Rechel J. Fifty. 2004. Effects of climate change on population persistence of desert-abode mountain sheep in California. Conserv. Biol. 18, 102–113 ten.1111/j.1523-1739.2004.00023.ten (doi:10.1111/j.1523-1739.2004.00023.x) [CrossRef] [Google Scholar]
67. Gilman S. Eastward., Urban M. C., Tewksbury J., Gilchrist G. W., Holt R. D. 2010. A framework for community interactions under climate alter. Trends Ecol. Evol. 25, 325–331 ten.1016/j.tree.2010.03.002 (doi:ten.1016/j.tree.2010.03.002) [PubMed] [CrossRef] [Google Scholar]
68. Urban M., Tewksbury J. J., Sheldon M. S. 2012. On a collision course: competition and dispersal differences create no-analogue communities and cause extinctions during climate change. Proc. R. Soc. B 279, 2072–2080 x.1098/rspb.2011.2367 (doi:ten.1098/rspb.2011.2367) [PMC costless commodity] [PubMed] [CrossRef] [Google Scholar]
69. Pearce-Higgins J. W., Dennis P., Whittingham M. J., Yalden D. Westward. 2010. Impacts of climate on casualty abundance business relationship for fluctuations in a population of a northern wader at the southern edge of its range. Glob. Alter Biol. 16, 12–23 ten.1111/j.1365-2486.2009.01883.10 (doi:10.1111/j.1365-2486.2009.01883.10) [CrossRef] [Google Scholar]
70. Rohr J. R., Raffel T. R. 2010. Linking global climate and temperature variability to widespread amphibian declines putatively caused by disease. Proc. Natl Acad. Sci. Usa 107, 8269–8274 ten.1073/pnas.0912883107 (doi:10.1073/pnas.0912883107) [PMC free article] [PubMed] [CrossRef] [Google Scholar]
72. Wolf S. G., Snyder M. A., Doak D. F., Croll D. A. 2010. Predicting population consequences of ocean climate change for an ecosystem sentinel, the seabird Cassin'due south auklet. Glob. Change Biol. sixteen, 1923–1935 10.1111/j.1365-2486.2010.02194.ten (doi:ten.1111/j.1365-2486.2010.02194.10) [CrossRef] [Google Scholar]
74. Glynn P. West., Mate J. L., Baker A. C., Calderon M. O. 2001. Coral bleaching and mortality in Panama and Ecuador during the 1997-1998 El Niño-Southern Oscillation event: spatial/temporal patterns and comparisons with the 1982–1983 result. Balderdash. Mar. Sci. 69, 79–109 [Google Scholar]
75. Graham N. A. J., Wilson South. K., Pratchett One thousand. S., Polunin Due north. V. C., Spalding Yard. D. 2009. Coral bloodshed versus structural plummet every bit drivers of corallivorous butterflyfish reject. Biodivers. Conserv. 18, 3325–3336 10.1007/s10531-009-9633-three (doi:10.1007/s10531-009-9633-3) [CrossRef] [Google Scholar]
76. Kiesecker J. M., Blaustein A. R., Belden L. K. 2001. Circuitous causes of amphibian population declines. Nature 410, 681–684 10.1038/35070552 (doi:10.1038/35070552) [PubMed] [CrossRef] [Google Scholar]
77. Timmermann A., Oberhuber J., Bacher A., Esch Thousand., Latif 1000., Roeckner E. 1999. Increased El Niño frequency in a climate model forced by future greenhouse warming. Nature 398, 694–697 10.1038/19505 (doi:10.1038/19505) [CrossRef] [Google Scholar]
78. Collins M., et al. 2010. The impact of global warming on the tropical Pacific Ocean and El Niño. Nat. Geosci. iii, 391–397 x.1038/ngeo868 (doi:x.1038/ngeo868) [CrossRef] [Google Scholar]
79. Pandolfi J. M., Connolly South. R., Marshall D. J., Cohen A. Fifty. 2011. Projecting coral reef futures under global warming and ocean acidification. Science 333, 418–422 x.1126/scientific discipline.1204794 (doi:10.1126/science.1204794) [PubMed] [CrossRef] [Google Scholar]
80. Hoegh-Guldberg O. 1999. Climate change, coral bleaching and the future of the world's coral reefs. Mar. Freshwater Res. 50, 839–866 10.1071/MF99078 (doi:10.1071/MF99078) [CrossRef] [Google Scholar]
83. Sagarin R. D., Barry J. P., Gilman S. E., Baxter C. H. 1999. Climate-related change in an intertidal customs over short and long time scales. Ecol. Monogr. 69, 465–490 10.1890/0012-9615(1999)069[0465:CRCIAI]2.0.CO;2 (doi:10.1890/0012-9615(1999)069[0465:CRCIAI]2.0.CO;2) [CrossRef] [Google Scholar]
84. Willis C. Yard., Ruhfel B., Primack R. B., Miller-Rushing A. J., Davis C. C. 2008. Phylogenetic patterns of species loss in Thoreau's woods are driven by climate change. Proc. Natl Acad. Sci. USA 105, 17 029–17 033 x.1073/pnas.0806446105 (doi:ten.1073/pnas.0806446105) [PMC complimentary article] [PubMed] [CrossRef] [Google Scholar]
85. Wethey D. S., Woodin S. A., Hilbish T. J., Jones Due south. J., Lima F. P., Brannock P. M. 2011. Response of intertidal populations to climate: effects of extreme events versus long term modify. J. Exp. Mar. Biol. Ecol. 400, 132–144 10.1016/j.jembe.2011.02.008 (doi:10.1016/j.jembe.2011.02.008) [CrossRef] [Google Scholar]
86. Dahlhoff Due east. P., Fearnley South. L., Bruce D. A., Gibbs A. Grand., Stoneking R., McMillan D. M., Deiner K., Smiley J. T., Rank Due north. E. 2008. Effects of temperature on physiology and reproductive success of a montane leaf protrude: implications for persistence of native populations enduring climate change. Physiol. Biochem. Zool. 81, 718–732 x.1086/590165 (doi:10.1086/590165) [PubMed] [CrossRef] [Google Scholar]
87. Tingley M. W., Beissinger S. R. 2009. Detecting range shifts from historical species occurrences: new perspectives on old data. Trends Ecol. Evol. 24, 625–633 ten.1016/j.tree.2009.05.009 (doi:ten.1016/j.tree.2009.05.009) [PubMed] [CrossRef] [Google Scholar]
88. Tingley M. W., Monahan Westward. B., Beissinger Due south. R., Moritz C. 2009. Birds track their Grinnellian niche through a century of climate alter . Proc. Natl Acad. Sci. USA 106, xix 637–xix 643 10.1073/pnas.0901562106 (doi:10.1073/pnas.0901562106) [PMC costless commodity] [PubMed] [CrossRef] [Google Scholar]
89. MacKenzie D. I., Nichols J. D., Royle J. A., Pollock K. H., Bailey L. 50., Hines J. Due east. 2006. Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Burlington, MA: Bookish Press [Google Scholar]
90. Charmantier A., McCleery R. H., Cole L. R., Perrins C., Kruuk L. Eastward. B., Sheldon B. C. 2008. Adaptive phenotypic plasticity in response to climate modify in a wild bird population . Science 320, 800–803 10.1126/science.1157174 (doi:10.1126/science.1157174) [PubMed] [CrossRef] [Google Scholar]
91. Boakes E. H., McGowan P. J. K., Fuller R. A., Chang-qing D., Clark Due north. East., O'Connor K., Mace K. M. 2010. Distorted views of biodiversity: spatial and temporal bias in species occurrence data. PLoS Biol. 8, e1000385. x.1371/journal.pbio.1000385 (doi:10.1371/journal.pbio.1000385) [PMC free article] [PubMed] [CrossRef] [Google Scholar]
92. Botts Eastward. A., Erasmus B. F. N., Alexander Thou. J. 2011. Geographic sampling bias in the South African Frog Atlas Project: implications for conservation planning. Biodivers. Conserv. 20, 119–139 10.1007/s10531-010-9950-six (doi:10.1007/s10531-010-9950-6) [CrossRef] [Google Scholar]
94. Peery M. Z., Beissinger S. R., Newman Southward. H., Burkett Eastward. B., Williams T. D. 2004. Applying the declining population epitome: diagnosing causes of poor reproduction in the marbled murrelet. Conserv. Biol. 18, 1088–1098 10.1111/j.1523-1739.2004.00134.ten (doi:x.1111/j.1523-1739.2004.00134.x) [CrossRef] [Google Scholar]
95. Beissinger S. R., Wunderle J. Thou., Jr, Meyers J. 1000., Saether B. E., Engen S. 2008. Anatomy of a bottleneck: diagnosing factors limiting population growth in the Puerto Rican parrot. Ecol. Monogr. 78, 185–203 10.1890/07-0018.one (doi:x.1890/07-0018.1) [CrossRef] [Google Scholar]
96. Daly C., Gibson W. P., Taylor G. H., Johnson G. L., Pasteris P. 2002. A knowledge-based arroyo to the statistical mapping of climate. Clim. Res. 22, 99–113 10.3354/cr022099 (doi:10.3354/cr022099) [CrossRef] [Google Scholar]
97. Buckley L. B., Urban Chiliad. C., Angilletta M. J., Crozier Fifty. One thousand., Rissler L. J., Sears 1000. W. 2010. Tin can mechanism inform species distribution models? Ecol. Lett. 13, 1041–1054 10.1111/j.1461-0248.2010.01479.ten (doi:10.1111/j.1461-0248.2010.01479.x) [PubMed] [CrossRef] [Google Scholar]
99. Richmond O. M. West., Hines J. E., Beissinger S. R. 2010. Two-species occupancy models: a new parameterization applied to co-occurrence of secretive rails. Ecol. Appl. 20, 2036–2046 x.1890/09-0470.1 (doi:10.1890/09-0470.1) [PubMed] [CrossRef] [Google Scholar]
100. Jones S. J., Mieszkowska Due north., Wethey D. South. 2009. Linking thermal tolerances and biogeography: Mytilus edulis (L.) at its southern limit on the eastward coast of the United states. Biol. Bull. 217, 73–85 [PubMed] [Google Scholar]
Manufactures from Proceedings of the Regal Society B: Biological Sciences are provided hither courtesy of The Royal Society
Source: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3574421/
Posted by: smithmonely.blogspot.com
0 Response to "How Did The Changing Climate Possibly Result In The Extinction Of These Animals?"
Post a Comment