diversity Review A Review of the Effects of Climate Change on Chelonians Christopher J. Butler Department of Biology, University of Central Oklahoma, Edmond, OK 73020, USA; [email protected] Received: 11 July 2019; Accepted: 13 August 2019; Published: 16 August 2019 Abstract: Climate change is occurring at an unprecedented rate and has begun to modify the distribution and phenology of organisms worldwide. Chelonians are expected to be particularly vulnerable due to limited dispersal capabilities as well as widespread temperature-dependent sex determination. The number of papers published about the effects of climate change on turtles has increased exponentially over the last decade; here, I review the data from peer-reviewed publications to assess the likely impacts of climate change on individuals, populations, and communities. Based upon these studies future research should focus on: (1) Individual responses to climate change, particularly with respect to thermal biology, phenology, and microhabitat selection; (2) improving species distribution models by incorporating fine-scale environmental variables as well as physiological processes; (3) identifying the consequences of skewed sex ratios; and (4) assessments of community resilience and the development of methods to mitigate climate change impacts. Although detailed management recommendations are not possible at this point, careful consideration should be given regarding how to manage low vagility species as habitats shift poleward. In the worst-case scenario, proactive management may be required in order to ensure that widespread losses do not occur. Keywords: chelonian; turtle; tortoise; climate change; species distribution model; ecological niche model; temperature-dependent sex determination 1. Introduction Anthropogenic climate change has numerous effects on biological communities, with many studies demonstrating ongoing changes in phenology, distribution, and community interactions [1–7]. In addition, anthropogenic climate change can reduce the amount of suitable habitat within the range of a species and thus increase the risk of extinction [8,9]. Climate change has been identified as one of the major threats to reptile populations [10]; the persistence of species may depend not only on the ultimate persistence of the climate, but also on the ability to keep pace with moving climates [11]. Turtles are one of the most threatened groups of vertebrates. According to the International Union for Conservation of Nature (IUCN) Red List [12], approximately 62.8% of chelonians (162 of 258 species) are either critically endangered (19.4%; n = 50), endangered (17.4%; n = 45) or vulnerable (30.0%; n = 65). The threats facing turtles are varied and include habitat loss, overexploitation, predation, invasive species, diseases, and climate change [10,13]. Poikilothermic animals, including turtles, may be particularly susceptible to the effects of anthropogenic climate change [14]. The possible effects of climate change on chelonians are varied and include potential skews in sex ratios [15], alteration of existing habitat [6,16], loss of suitable habitat [17], and extinction [18]. In addition, turtles and tortoises have limited vagility and may not be able to keep pace with forecasted climatic changes [10]. The impacts of climate change may vary depending upon the life-history stage; many aspects of chelonian embryonic development are influenced by hydrology and temperature while they are in the nest [19]. Anthropogenic climate change could affect individual growth rates [20], fecundity [21], reproductive phenology [22], sex ratios via temperature-dependent Diversity 2019, 11, 138; doi:10.3390/d11080138 www.mdpi.com/journal/diversity Diversity 2019, 11, x FOR PEER REVIEW 2 of 21 Diversity 2019, 11, 138 2 of 22 while they are in the nest [19]. Anthropogenic climate change could affect individual growth rates [20], fecundity [21], reproductive phenology [22], sex ratios via temperature-dependent sex sexdetermination determination [15], [15 and], and predation predation rates rates [23,24]. [23,24 Alth]. Althoughough turtles turtles have have survived survived previous previous periods periods of ofclimate climate change, change, the the existing existing rate rate of of change change isis far far more more rapid rapid and and turtles turtles may may not not be be able able to respond inin time,time, duedue inin partpart toto theirtheir longlong generationgeneration timestimes [[25].25]. Much ofof the the existing existing research research on on climate climate change change and and chelonians chelonians has focused has focused on the on eff ectsthe ofeffects climate of changeclimate onchange marine on turtles.marine turtles. Although Although the seven the species seven species of sea turtleof sea ( Cheloniaturtle (Chelonia mydas, Carettamydas, Caretta caretta, Eretmochelyscaretta, Eretmochelys imbricata imbricata, Dermochelyis, Dermochelyis coriacea, Lepidochelyscoriacea, Lepidochelys kempii, L. kempii olivacea, L., andolivaceaNatator, and depressus Natator) representdepressus) approximatelyrepresent approximately only 2% of only the existing2% of the chelonian existing specieschelonian [12 species], 52.1% [12], of published 52.1% of published papers on turtlespapers andon turtles climate and change climate between change 1991 between and 2017 1991 focused and 2017 on seafocused turtles on(n sea= 335 turtles and (n 643 = respectively;335 and 643 Figurerespectively;1). Hawkes Figure et1). al. Hawkes [ 25,26 ]et provided al. [25,26] a provided review of a review existing of papers existing on papers sea turtles on sea and turtles climate and change.climate change. To date, To however, date, however, there has there not been has anot review been ofa thereview effects of the of climate effects changeof climate on freshwaterchange on orfreshwater terrestrial or chelonians. terrestrial chelonia Additionally,ns. Additionally, the number the of number papers published of papers published on climate on change climate eff changeects on turtleseffects andon turtles tortoises and have tortoises increased have moreincreased than more four-fold than since four-fold the publication since the publication of this review of this (Figure review1), so(Figure an updated, 1), so an comprehensive updated, comprehensive review of data review published of data on the published existing andon the predicted existing eff andects ofpredicted climate changeeffects of on climate sea turtles, change as wellon sea as turtles, freshwater as well and as terrestrial freshwater chelonians, and terrestrial is warranted. chelonians, is warranted. Figure 1.1. The number of published papers related to climate change and chelonianschelonians has increasedincreased substantially duringduring the the 21st 21st century. century. This This figure figure summarizes summarizes the the number number of published of published studies studies per year per (resultingyear (resulting from from an ISI an (Institute ISI (Insti fortute Scientific for Scientific Information) Information) Web ofWeb Science of Science search search on 8 Auguston 8 August 2019) containing2019) containing the search the termssearch “turtles terms “turtles OR tortoises OR tortoi OR chelonian”ses OR chelonian” and “climate and change “climate or globalchange warming”, or global aswarming”, well as the as search well as terms the “seasearch turtle terms OR “sea Chelonia turtle OR OR Caretta Chelonia OR EretmochelysOR Caretta OR OR Eretmochelys Dermochelyis OR LepidochelysDermochelyis OROR Natator”Lepidochelys and “climate OR Natator” change and or “climate global warming”. change or global warming”. 2. Current Effects Effects A hierarchical classificationclassification of ecology, from smallestsmallest to largest,largest, includes cells, organisms, populations, communities,communities, ecosystems, landscapes, biomes, an andd the biosphere, although other classificationclassification schemesschemes have have been been proposed proposed [27]. However,[27]. However, most ecological most ecological studies focus studies on organisms,focus on populations,organisms, populations, and communities and communities [28]. Anthropogenic [28]. Anthropogenic climate change climate could change conceivably could a ffconceivablyect each of theseaffect levels,each of with these eff ectslevels, on individualswith effects leadingon individuals to changes leading in populations, to changes which in populations, in turn could which lead toin changesturn could in communities.lead to changes There in havecommunities. been numerous There studieshave been on thenumerous effects of studies climate on change the effects for each of ofclimate these levelschange in for a variety each of of these organisms levels over in a the variet pasty threeof organisms decades, withover manythe past of thethree studies decades, exploring with themany potential of the estudiesffects of exploring climate change the potential during theeffects second of climate half of thechange 21st during century. the There second have half also of been the Diversity 2019, 11, 138 3 of 22 a few studies exploring the current effects of climate change on chelonians. The following summarizes research showing how climate change currently affects individuals, populations, and communities. 2.1. Individuals Climate change could conceivably modify resource availability, reducing or changing the prey base and affecting individual growth rates or survivorship. In addition, phenotypic and behavioral plasticity could also potentially ameliorate or