A short review of the roles of climate and man in mammal extinctions during the Anthropocene

Rend. Fis. Acc. Lincei (2014) 25:95 99 DOI 10.1007/s12210-013-0240-6 ANTHROPOCENE - NATURAL AND MAN-MADE ALTERATIONS OF THE EARTH A short review of the roles of climate and man in mammal extinctions during the Anthropocene Giovanni Amori Spartaco Gippoliti Luca Luiselli Received: 20 March 2013 / Accepted: 7 May 2013 / Published online: 22 May 2013 Ó Accademia Nazionale dei Lincei 2013 Abstract The evolutionary history of plant and animal species has been deeply influenced by both climate changes and human actions. Human actions have been particularly heavy during the Anthropocene, when over 250 mammal species became extinct, mostly on islands. Here, we shortly review the existing literature, and test whether the various mammalian orders are all equally prone to extinction risks. We concluded that species belonging to the orders Rodentia, Primates, and Artiodactyla were more prone to become extinct, whereas those belonging to the orders Chiroptera and Carnivora were less. Surprisingly, apparently IUCN red list placed higher conservation concerns for the species belonging to the mammalian orders which are globally least prone to become extinct during the Holocene. Keywords Anthropocene Holocene Mammals Extinctions Climate change Review This contribution is the written, peer-reviewed version of a paper presented at the conference Anthropocene Natural and man-made alterations of the Earth s fragile equilibrium, held at Accademia Nazionale dei Lincei in Rome on November 26 27, 2012. G. Amori (&) CNR Institute of Ecosystem studies, Viale dell Università 32, 00181 Rome, Italy e-mail: giovanni.amori@uniroma1.it S. Gippoliti Viale Liegi 48A, 00198 Rome, Italy L. Luiselli Centre of Environmental Studies Demetra s.r.l, Via Olona 7, 00198 Rome, Italy 1 Climate, humans, and extinctions: a short introduction The evolutionary history of plant and animal species has been deeply influenced by climate changes (e.g. Hewitt 1996, 1999, 2004; Easterling et al. 2000). Indeed, climate is very important in determining the distribution ranges and in producing spatial isolation between populations with consequent speciation processes (Hewitt 2001, 2004). For example, Ice ages have always been factors affecting the distribution of many plants and animals (Cagnin et al. 1998; Battisti 2006), and in Europe the more adapted species perished and other found refuge moving to the south along the three Mediterranean peninsulas (Hewitt 2001, 2004). Repeated contraction and expansion, coupled with the existence of physical barriers would accumulate genome differences and adaptations, protected from mixing by hybrid zones, and such a composite mode of speciation could apply to many organisms (Hewitt 2001). Phylogeography studies confirmed the assumption concerning southern refugia and also the existence of other refugia (in Central Europe), and the existence of multiple refugia in the same Southern Peninsula (Grill et al. 2009; Vega et al. 2010). These patterns are well documented, for instance, for several species of Italian small mammals, i.e. Neomys spp., Microtus spp., Myodes glareolus, Sciurus vulgaris (Castiglia et al. 2007, 2008; Grill et al. 2009; Colangelo et al. 2012). However, the extinctions of several mammal species and populations began in the late Pleistocene and early Holocene, when some species (i.e. Coelodonta antiquitatis, Ursus spelaeus, Megaloceros giganteus, Mammuthus primigenius) disappeared mainly due to climate change, with humans playing probably only a relatively marginal

96 Rend. Fis. Acc. Lincei (2014) 25:95 99 role in their extinctions (e.g., Nogues-Bravo et al. 2008). An interesting evidence of the somewhat limited role that humans had on the extinction of some species is that there were several cases of extinctions (due to climatic reasons) in portions of the ranges where humans were absent. For instance, woolly rhinoceros (C. antiquitatis) went extinct despite their range never overlapped that of humans (Lorenzen et al. 2011). Conversely, a comparatively larger number of species became extinct in ways more clearly linked to human activities. For instance, this was the case everywhere Homo sapiens sapiens started to establish the first human settlements, about VI millennium BC (Turvey 2009). In that period, the man shifted from a nomadic style of life into an agricultural one, and this has produced dramatic large-scale changes in land-use and habitat loss, thus affecting both directly (via hunting) and indirectly (deforestation and habitat loss) the various mammal species (Thomas 1956; Turvey 2009). Just to give an idea of what has happened, it is just enough to consider that, during the Roman Empire age, the daily consumption of fire wood was about 10 tons only for satisfying the needs of the Baths of Caracalla, with a storage reserve of 7,000 tons, i.e. the amount requested for 7 months (Pratesi 2001; Angela 2010). This amount of fire wood was just a fraction of the daily needs of Roman baths, given that there were 11 bath installations of the same size as Caracalla s ones and about 800 of smaller size only in Rome, with several thousands in the whole of the empire (Angela 2010). Since then, the main human activities which have been considered to cause extinctions were overhunting, introduction of diseases, increased interspecific competition, habitat destruction, and introduction of exotic species. All of these activities have increased dramatically over time (Vigne 1992). In this regard, an interesting example is given by the extinction of endemic mammal species in Corsica and Sardinia. Indeed, it has been demonstrated that, after the arrival of humans in these islands about 8,500 years ago, there was a relatively rapid extinction of the entire autochthonous mammalian fauna (represented by five endemic species, i.e. Episoriculus corsicanus, Rhagamys orthodon, Tyrrhenicola henseli, Prolagus sardus, Megaloceros cazioti) with the successful introduction of 27 allochthonous species (Fig. 1, Vigne 1992). The only endemic terrestrial mammal species that was able to survive for a relatively long time after human occupation was P. sardus, a lagomorph species of the family Ochotonidae. This species survived until 1774 on the small Sardinian island of Tavolara (MacPhee 1999), whereas it was totally extinct elsewhere since hundreds of years (Turvey 2009). Another evidence of direct human impact on Mediterranean Islands mammals is that, as suggested by Gippoliti and Amori (2006), endemic lineages may survive among non-hunted species, such as bats, as proved by the recent description of Plecotus sardus (Mucedda et al. 2002). 2 Is the extinction rate even among all mammalian groups? An interesting and debatable issue is to test which are the mammalian orders that are genuinely (i.e., intrinsically) more prone to become extinct. To test this fascinating issue, we have compared the number of extinct species during the Holocene by order (based on available literature) versus the number of extant species (Wilson and Reeder 2005). Fig. 1 Schematic view of the extinction of endemic taxa and invasion of allochthonous taxa after the beginning of human occupation in Corsica and Sardinia (modified from Vigne 1992)

Rend. Fis. Acc. Lincei (2014) 25:95 99 97 Table 1 Number of mammal species extinct during the Holocene (source: Turvey 2009) and still extant (Wilson and Reeder 2005) Order No. extinct species No. extant species Didelphimorpha 1 87 Dasyumorpha 2 71 Peramelemorpha 5 21 Diprodontia 11 143 Afrosoricidae 1 51 Bibymalagasia? 2 0 Proboscidea 2 3 Sirenia 1 5 Pilosa 16 10 Primates 22 376 Lagomorpha 2 92 Soricomorpha 14 428 Chiroptera 24 1,116 Carnivora 6 286 Perissodactyla 1 17 Artiodactyla 15 240 Cetacea 1 84 Rodentia 125 2,277 Based on the body of available literature (see Turvey 2009 for the raw dataset), a total of 249 mammal species went extinct during the Holocene (251 if we include also the Bibymalagasia), whereas 5,307 are extant (Table 1). Out of these 251 extinct mammal species, 91.7 % occurred on islands, and only 8.3 % in continental lands. The observed number of extinct species was significantly uneven among groups (v 2 =.4, df = 16, P \ 0.0001), with rodents accounting for 49.8 % of the total extinct species. If we take into account the species richness of the various mammalian orders (Table 1), it resulted that there were significant differences between observed and expected number of extinct species by order (v 2 = 593.4, df = 16, P \ 0.0001). If we look at the patterns in more detail (Fig. 2), it resulted that the number of extinct species was significantly (1) higher than expected in Rodentia, Primates, and Artiodactyla, and (2) lower than expected in Chiroptera and Carnivora. For all other orders, the observed and expected numbers of extinct species did not differ significantly. The number of threatened taxa (according to IUCN, 2012) was significantly uneven (v 2 = 2,102, df = 16, P \ 0.0001) among mammalian groups, and, interestingly did not parallel the patterns of extinction presented above. Indeed, there was a significantly negative linear relationship between percent of threatened species by order and percent of extinct species by order (r =-0.514, P \ 0.0001; Fig. 3). Looking more in detail to the groups that were significantly more/less prone to extinction than expected (see above), the percent of extant carnivore species endemic to islands was 9.4 % (n = 286), species in total; Table 2, that of Artiodactyla was 9.2 % (n = 240), that of rodents was 17 % (n = 2,777), and that of primates was 26.6 (n = 376). The frequencies of endemic island species were significantly higher in rodents and primates than in carnivores and Artiodactyla (in all cases P \ 0.01 at v 2 test), whereas there was no difference between carnivores and Artiodactyla. Fig. 2 Numbers of observed extinct species by order and expected number of extinct species by order taking into account the relative species richness of each order

98 Rend. Fis. Acc. Lincei (2014) 25:95 99 Fig. 3 Relationship between (arc-sin) percent of threatened species by order and (arc-sin) percent of extinct species by order. For the statistical details, see the text picture of threatened species as emerging from IUCN (2012) database. That is apparently, IUCN conveys an emphasis on the conservation needs of the various mammalian orders which is opposite to the extinction trends which have characterized the whole class Mammalia during the Holocene. Similarly, Amori and Gippoliti (2000) showed that there was a total independence between percent of threatened species by order and percentage of devoted peer-review articles in leading conservation journals. Thus, also the present study confirmed the mismatch between conservation needs and conservation attention by relevant agencies (including IUCN), thus possibly with deleterious effects on global conservation strategy. Our analysis, however, has some complications, the main one being the fact that extinctions are not evenly distributed across the world, with island species being much more exposed to extinction than mainland species (Turvey 2009). Thus, it may be possible that groups such as rodents are overly represented in the extinction list because more prone to show insular speciation events. Table 2 Number of threatened species (CR, E, VU) and percent of threatened species on the total species richness of each group, in mammals Order Number of threatened species Didelphimorpha 8 8.42 Dasyumorpha 12 16.21 Peramelemorpha 6 27.27 Diprodontia 45 30.82 Afrosoricida 17 31.48 Proboscidea 1 50.00 Sirenia 4 80.00 Pilosa 2 20.00 Primates 201 48.43 Lagomorpha 17 18.27 Soricomorpha 84 18.66 Chiroptera 177 15.39 Carnivora 71 24.91 Perissodactyla 13 81.25 Artiodactyla? Cetacea 109 33.13 Rodentia 358 15.87 Data source: IUCN (2012) Percentage of threatened species Hence, our analysis documented that (1) some mammalian orders were theoretically more exposed to the risk of extinction (if we consider that their respective numbers of extinct taxa is higher than expected based on their relative species richness), and (2) the expected patterns of extinction exposure were inversely related to the overall 3 Conclusions Our short review pointed out that climate changes have always produced extinctions, range shifts, and speciations. However, during the Anthropocene, humans have heavily impacted the mammalian fauna, amplifying and accelerating the actions of climate. It is also noteworthy that not all the mammalian groups are affected in the same way by the extinction risk, and that the leading conservation organizations (i.e. IUCN) did not apparently select the most fragile groups as those requiring the main preservation attention. However, there is a recent awareness about species susceptibility to both climate change and human activity impacts (e.g., Vié et al. 2009), and it is hoped that conservation actions will help to mitigate the extinction rates that have been characterizing the Anthropocene. References Amori A, Gippoliti S (2000) What do mammalogists want to save? Ten years of mammalian conservation biology. Biodiv Conserv 9:785 793 Angela A (2010) Impero. Viaggio nell Impero di Roma seguendo una moneta, Mondadori Battisti C (2006) Peninsula effect and Italian peninsula: materials for a review and implications in applied biogeography. Biogeographia 27:153 188 Cagnin M, Moreno S, Aloise G, Garofalo G, Villafuerte R, Gaona P, Cristaldi M (1998) Comparative study of Spanish and Italian terrestrial small mammal coenoses from different biotopes in Mediterranean peninsular tip regions. J Biogeogr 25:1105 1113

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