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Temporal Changes in Cranial Size in South African Vlei Rats (Otomys): Evidence for the 'Third Universal Response to Warming'

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Temporal Changes in Cranial Size in South African Vlei Rats (Otomys): Evidence for the 'Third Universal Response to Warming' African Zoology ISSN: 1562-7020 (Print) 2224-073X (Online) Journal homepage: http://www.tandfonline.com/loi/tafz20 Temporal changes in cranial size in South African vlei rats (Otomys): evidence for the ‘third universal response to warming’ Aluwani Nengovhela, Roderick M Baxter & Peter J Taylor To cite this article: Aluwani Nengovhela, Roderick M Baxter & Peter J Taylor (2015): Temporal changes in cranial size in South African vlei rats (Otomys): evidence for the ‘third universal response to warming’, African Zoology To link to this article: http://dx.doi.org/10.1080/15627020.2015.1052014 View supplementary material Published online: 24 Jul 2015. Submit your article to this journal Article views: 13 View related articles View Crossmark data Full Terms & Conditions of access and use can be found at http://www.tandfonline.com/action/journalInformation?journalCode=tafz20 Download by: [University of Stellenbosch] Date: 13 October 2015, At: 03:10 African Zoology 2015: 1–7 Copyright © Zoological Society Printed in South Africa — All rights reserved of Southern Africa AFRICAN ZOOLOGY This is the final version of the article that is ISSN 1562-7020 EISSN 2224-073X published ahead of the print and online issue http://dx.doi.org/10.1080/15627020.2015.1052014 Temporal changes in cranial size in South African vlei rats (Otomys): evidence for the ‘third universal response to warming’ Aluwani Nengovhela1,2, Roderick M Baxter1,2 and Peter J Taylor2,3* 1 Department of Ecology and Resource Management, School of Environmental Sciences, University of Venda, Thohoyandou, South Africa 2 South African Research Chair on Biodiversity Value and Change in the Vhembe Biosphere Reserve, School of Mathematics and Natural Sciences, University of Venda, Thohoyandou, South Africa 3 Core Team Member of the Centre for Invasion Biology, Stellenbosch University, Stellenbosch, South Africa. * Corresponding author, email: [email protected] Using museum collections and recently collected specimens we studied geographical and temporal (from 1906 to 2013) changes in skull size of two sibling species of rodents, Otomys auratus and O. angoniensis, in northern South Africa occupying distinct temperate grassland (O. auratus) and subtropical savanna (O. angoniensis) biomes. We hypothesised that cranial size should vary in space and time within species according to Bergmann’s Rule, which predicts an inverse relationship between body size and temperature. We used the greatest length of the skull (GLS) as a robust indicator of body size. Cranial size of both O. auratus and O. angoniensis decreased significantly over the past 100 years, as expected given historical evidence of warming across northern South Africa since the 1950s. In terms of geographical patterns, GLS was inversely correlated with both latitude and longitude in O. auratus but these trends were correlated with annual rainfall rather than mean annual temperature. Conversely, cranial size of O. angoniensis was weakly positively correlated with longitude but with no climatic variables. Our results demonstrate rapid morphological changes in two herbivorous South African rodents over the past 100 years. Whilst the general decline in size with time in relation to increased temperature is consistent with Bergmann’s Rule, multiple drivers may underlie geographical trends in the two species. Keywords: Bergmann’s Rule, body size, climate change, morphometric variation, Muridae, South Africa Introduction Global surface temperature has been reported to have et al. 2014). Similarly, high rates of local extinction due increased by 0.08–0.14 °C per decade between 1950 to climate change have been predicted for populations of and 2012 and it is predicted in many scenarios to rise by montane vertebrates, particularly hydrophilous amphib- 2 °C by 2100 (IPCC 2014). In southern Africa over the last ians and vertebrates of montane regions of Latin America century, annual minimum and maximum temperatures have (McCain and Colwell 2011). Examples of phenological increased by an average of 0.057 °C and 0.046 °C, respec- impacts include earlier arrival of Australian migratory birds Downloaded by [University of Stellenbosch] at 03:10 13 October 2015 tively, per decade (Davis 2011). Rising temperatures have (Beaumont et al. 2006) and earlier egg laying of 20 species also been reported in South Africa (Kruger and Shongwe of British birds (Crick et al. 1997). 2004), particularly in Limpopo province (Tshiala et al. 2011). Morphological changes due to global warming have been Anthropogenic climate warming is one of the main threats reported in a number of species on different continents to biodiversity today (Parmesan 2006). This warming and in both terrestrial and aquatic environments (Gardner affects phenology, distribution and morphology of species et al. 2011). Studies have primarily used skull length as (Hughes 2000; Eastman et al. 2012). For instance, distri- a measure or proxy for body size in both museum and bution margins of different montane species have been modern specimens (e.g. Yom-Tov and Yom-Tov 2004; observed to be shifting towards the pole and upward in Pergams and Lawler 2009; Eastman et al. 2012; Tomassini elevation where they are tracking favourable climatic et al. 2014). These morphological changes can sometimes conditions (Hughes 2000; Parmesan and Yohe 2003; Root be explained by Bergmann’s (1847) zoogeographical et al. 2003; Mulungu et al. 2008). This kind of shift has also rule, which states that animal body size decreases with been reported for small mammals in Yosemite National Park increasing temperature. Although this generalisation has (Moritz et al. 2008). Projected range shifts due to climate been mostly tested with respect to variation in latitude and change in range-restricted species may result in high risk of elevation (i.e. spatially), it should also apply temporally in extinction as reported for the Sokoke Scops Owl in Kenya the case of global warming associated with climate change. and north-eastern Tanzania (Monadjem et al. 2012) and for The debate over which factor(s) ultimately determine body the Perote ground squirrel in Mexico (García-Domínguez size has not yet been settled (Yom-Tov and Geffen 2006). African Zoology is co-published by NISC (Pty) Ltd and Taylor & Francis 2 Nengovhela, Baxter and Taylor There have been disagreements between authors on the Methods authenticity of Bergmann’s rule (Scholander 1955; McNab 1971; Calder 1984 in Millien et al. 2006), and some studies Geographic scope and specimens sampled conform to the rule while others do not. For example, A total of 254 skulls of Otomys were measured comprising Yom-Tov (2001) observed a body mass decline in four 230 (111 O. angoniensis and 119 O. auratus) from the species of Israeli passerine birds (Prinia gracilis, Passer Ditsong National Museum (formerly Transvaal Museum: domesticus, Pycnonotus xanthopygos and Sylvia melano- TM) from Gauteng, North West, Mpumalanga and Limpopo cephala) between the years 1950 and 1999. On the other provinces (59 localities for O. auratus and 86 localities hand, Yom-Tov et al. (2006) also reported a linear increase for O. angoniensis) and 24 (19 O. angoniensis and five with time in body weight of four species of British passerine O. auratus) newly collected specimens from Limpopo birds. The body size of ground squirrels Spermophilus province (Soutpansberg and Waterberg ranges) and beecheyi has been reported to have increased in northern Gauteng province (Rietvlei Nature Reserve) (Figure 1). California, where it is wetter and cooler than it was during The recently collected specimens were all deposited in the the last glacial maximum (LGM) when it was much drier mammal collection of the Durban Natural Science Museum. and colder, thus conforming to the expected pattern of Standard small mammal live-trapping (with Sherman traps) Bergmann’s rule, but this has been attributed to changes in and specimen preparation procedures were used to collect precipitation not temperature (Blois et al. 2008). Yom-Tov these specimens under collecting permits from the Limpopo and Yom-Tov (2004) showed a temporal increase in skull Department of Environmental Affairs and Tourism (LEDET) size of the Japanese rodent Apodemus speciosus. In (permit no. 001-CPM403-00010), and for Rietvlei Nature the masked shrew Sorex cinereus of Alaska, Yom-Tov Reserve, with the permission of the Tshwane Municipality and Yom-Tov (2005) reported a decrease of body size and Gauteng Department of Agriculture and Rural associated with high latitudes and high January minimum Development. Capture and handling followed the guidelines temperatures, thus contradicting Bergmann’s rule, and prescribed by the American Society of Mammalogists (Sikes an identical pattern was found in five Eurasian species of et al. 2011). shrews (Sorex) by Ochocińska and Taylor (2003). These The museum sample included specimens collected changes in body size were attributed to scarcity of food in between 1906 and 2003 for O. angoniensis and between far northern climates selecting for small body size since 1907 and 1994 for O. auratus. Our recent collections smaller shrews require less food. Changes in tempera- (2010–2013) from the Soutpansberg and Rietvlei allowed ture are therefore not the only factors that affect animal comparisons with historical samples from the same localities body size. There are other factors such as increased food collected in 1923 and 1970–1971, respectively. Sampling availability (Yom-Tov 2003; Yom-Tov and Yom-Tov 2005; across time and space was random and fairly representa- Eastman et al. 2012), predation (Yom-Tov et al. 2002) and tive of all regions and time periods (Figure 1, Supplementary anthropogenic effects such as increased urbanisation and Tables S1 and S2; see also scatterplots in Results). We human populations (Yom-Tov 2003; Pergams and Lawler could not detect any biases due to sampling of particular 2009; Tomassini et al. 2014). The murid tribe Otomyini is endemic to Africa (Taylor et al. 2004a). Most species of the genus Otomys are restricted to relict montane distributions, resulting in high levels of LEGEND AFRICA O. angoniensis regional endemism and widespread disjunction (Clausnitzer O.
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