No recent temporal changes in body size of three Danish rodents
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1 Acta Theriol (2012) 57:59 63 DOI /s y ORIGINAL PAPER No recent temporal changes in body size of three Danish rodents Yoram Yom-Tov & Shlomith Yom-Tov & Thomas Secher Jensen & Hans Baagoe Received: 5 May 2011 /Accepted: 4 July 2011 /Published online: 21 July 2011 # Mammal Research Institute, Polish Academy of Sciences, Białowieża, Poland 2011 Abstract We used museum collections to study temporal trends of possible changes in skull size, body mass and body length in three species of rodents in Denmark. Skulls of adult Microtus agrestis, Apodemus flavicollis and Apodemus sylvaticus, collected between 1895 and 2004, 1847 and 2002, and 1895 and 2002, respectively, were measured and data on body mass and length were taken from the museum registers. Principal component (PC) analysis was used to combine data of the four skull measurements taken. We tested the relationship of sex, latitude, longitude, month and year of collection to PC1 by a General Linear Model (GLM). PC1, body length and body mass of M. agrestis significantly increased from west to east. In addition, PC1, body mass and body length of M. agrestis declined from summer (August) through autumn and winter to spring (March), probably due to the decline in food availability towards winter. None of the other factors examined (sex, latitude and year) were significantly related to body size. PC1 of A. flavicollis and A. sylvaticus was not significantly related to any of the environmental factors examined. Communicated by: Jan M. Wójcik Y. Yom-Tov (*) : S. Yom-Tov Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel yomtov@post.tau.ac.il T. S. Jensen Natural History Museum, Aarhus, Denmark H. Baagoe Natural History Museum of Denmark and Zoological Museum, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen ø, Denmark Keywords Denmark. Rodents. Body size changes Introduction Adult body size may vary geographically and over time, and may be influenced by several factors, including nutrition during the growth period, inter- and intra-specific competition, predation and ambient temperature (Mayr 1970; Lindstrom 1999; Gosler et al. 1995). Recently, McNab (2010) argued that the tendency of mammals to increase or decrease body size geographically and temporally depends on the abundance, availability and size of resources, and termed this pattern as the resource rule. In homeothermic animals, a change in skull size and body mass can develop rather rapidly, as reported for animals introduced into new environments. For example, within 50 years after its introduction into New Zealand, the body size of the brushtail possum Trichosurus vulpecula correlated with ambient temperature, as it does in Australia from where it was introduced (Yom-Tov et al. 1986). Changes in body size may occur within a few years due to rapid environmental changes. Smith et al. (1998) found that body mass of Neotoma woodrats in New Mexico decreased significantly within 8 years, apparently as a reaction to an increase in ambient temperature. Most studies that documented temporal size trends were carried out on mammalian carnivores and birds, with only a few (Smith et al. 1998; Pergams and Ashley 2001; Wójcik et al. 2006) published on rodents (Yom-Tov and Geffen 2011). Yom-Tov and Geffen (2011) argued that animal body size acts much like a barometer, fluctuating in parallel with environmental changes, and specimens preserved in museums may serve as archives of past conditions that affected animal size. However, museum collections were rarely
2 60 Acta Theriol (2012) 57:59 63 gathered in a planned manner, and sample sizes for various species vary greatly between years and localities. This disadvantage may affect the power of analyses, and often make the interpretation of the results difficult and speculative. Authors of studies such as the present one that are based on museum collections have to be aware of this disadvantage. Denmark lies between about 8 15 E and N and comprises a peninsula (Jutland) and many islands, the largest of which is Zealand (where Denmark's capital, Copenhagen, is located). Over the last few centuries, the Danish landscape has undergone major changes, and today it consists in fragmented natural habitats dispersed among cultivated areas (Schmidt and Jensen 2003). Using data on body length of Danish mammals from the literature, Schmidt and Jensen (2003) have shown that several species of Danish mammals have undergone a change in body length during the last 175 years, with the smaller ones generally increasing in size; and they attributed these changes to habitat fragmentation. Yom-Tov et al. (2003, 2010) showed that the Danish red fox (Vulpes vulpes), Eurasian badger (Meles meles) and stone marten (Martes foina) all revealed variations in size during the twentieth century. The field vole Microtus agrestis is a small rodent common in central and northern Europe. It inhabits grasslands, meadows, the margins of fields and forestry plantations, but may also be found in hedgerows, dunes, open moorland and blanket bogs (Macdonald and Barrett 1993; Macdonald and Tattersall 2001). Its diet consists of grasses and herbaceous plants. Mice of the genus Apodemus are small Palearctic rodents that live mainly in woodland, but also occupy other habitats such as forests and cultivated fields. The wood (or longtailed) mouse Apodemus sylvaticus is a widely distributed species. In Europe, it occurs in woodland, arable land and gardens, and may also move into human habitations in the fall and winter. It is an opportunistic species and eats a varied diet of seeds, seedlings, buds, fruit, nuts, fungi, moss, snails, insect larvae, earthworms and centipedes (Macdonald and Barrett 1993; Macdonald and Tattersall 2001). In Europe, body size of the wood mouse varies geographically and increases from north to south, contrary to Bergmann's rule (Alcantara 1991). This phenomenon is related to regions of sympatry and allopatry with the yellow-necked mouse (Apodemus flavicollis), and may also be related to character displacement (Alcantara 1991), with the larger yellow-necked mouse negatively affecting the smaller wood mouse. The yellow-necked mouse is common in Europe, and is very similar in appearance to the wood mouse (A. sylvaticus), but generally larger than the latter. This species inhabits mature broadleaved woodlands, as well as orchards, arable land, field margins, wooded gardens, hedgerows and buildings in rural areas (Macdonald and Tattersall 2001). Its diet consists of seedlings, buds, fruit and about 10% invertebrates (Macdonald and Barrett 1993; Macdonald and Tattersall 2001). We used the above three species of rodents to study temporal and geographic trends of skull size, body mass and body length in Denmark during the last 150 years and geographically in Denmark. Methods Skulls of 227 adult M. agrestis, 336 adult A. flavicollis and 275 adult A. sylvaticus were measured at the Zoological Museum of Copenhagen and the Aarhus Natural History Museum. Adults were defined by means of tooth wear and fusion of the cranial bones. Skulls of A. flavicollis were collected between 1895 and 2002, A. sylvaticus between 1847 and 2002 and M. agrestis between 1895 and The number of specimens collected annually ranged between 1 and 22 (with one exception of 147 A. flavicollis collected in 1 year), and the number of years (and mean number of specimens per year) for which there were 36 (9.1), 40 (6.3) and 29 (5.5) specimens for A. flavicollis, A. sylvaticus and M. agrestis, respectively. Hence, between only a quarter and a third of the years of the study period was represented in our sample. For each specimen, we noted (from its label or museum catalogue) its sex, locality and date of collection, and when available, also body mass and body length. Data of body mass and length were available for shorter periods and fewer specimens: for A. flavicollis between 1910 and 2002 (162 specimens), for A. sylvaticus between 1937 and 2002 (25 specimens) and for M. agrestis between 1938 and 2002 (126 specimens). However, for both species of Apodemus most (more than 87%) of the data on body mass and length were for only 3 years ( ). Due to this bias, for both Apodemus species we did not use data on body mass and length. Using digital callipers, four measurements were taken from each skull to an accuracy of 0.01 mm: greatest length (GTL), zygomatic breadth (ZB), narrowest width of the skull across the interorbital region (IC) and the length of the upper cheek teeth row (UpM). We used principal component analysis (PCA) to combine the information of the four skull measurements (log transformed for normality) into a single variable, and (log transformed) body mass and body length. General Linear Models (GLM) were used to test the relationship of sex (dummy variable), latitude, longitude, year and month of collection on PC1, and for the vole also for body mass and body length. The monthly variation in size was presented by the sinusoidal component Sin(2 pi I/12) where I=1
3 Acta Theriol (2012) 57: , and 1=January, 2=February, etc., which was found to fit well the monthly effect Results The PCA clumped the four skull parameters (GTL, ZB, IC and UpM, all log transformed) into a single factor. For the three species, Eigenvalue was , and and the proportion of variance explained by that factor (PC1) was 56.2%, 65.3% and 56.0% for M. agrestis, A. flavicolli and A. sylvaticus, respectively. We then examined the effects of sex, latitude, longitude, year and month of collection on PC1 for the three species. Residual body length Aug. Dec. Month Mar. M. agrestis PC1 was significantly related to body mass (n=125, F= , R 2 =0.2484, P<0.0001) and body length (n=119, F= , R 2 =0.1915, P<0.0001), and body mass and length were significantly related to each other (n=121, F= , R 2 =0.6887, P<0.0001). Results of GLMs indicated that PC1, body length and body mass were significantly related to longitude (Fig. 1), increasing from west to east. PC1, body mass and body length of M. agrestis declined from the summer through autumn and winter to spring (Fig. 2, Table 1; for PC1: likelihood test # 2 5 ¼ 29:7398, P<0.0001; for body length: likelihood test # 2 5 ¼ 47:2826, P<0.0001; for body mass: likelihood test # 2 5 ¼ 23:3575, P<0.0001). A. flavicollis Results of GLM indicated that PC1 was significantly related only to sex and no temporal change was detected Residual body length Longitude Fig. 1 Regression plot of the relationship between body length (corrected for sex, latitude, month and year of collection) and longitude in M. agrestis. F 1,125 = , R 2 =0.1274, P< Fig. 2 Regression plot of the relationship between body length (corrected for sex, latitude, longitude and year of collection) and month (in its sinusoidal component) in M. agrestis. F 1,125 = , R 2 =0.0951, P= (Table 2; likelihood test # 2 5 ¼ 17:9177, P=0.0031). Removal of sex rendered the relationship of all other factors insignificant (likelihood test # 2 4 ¼ 6:4099, P=0.1706). The insignificant results had low power (<0.16) and it is possible that they are due to small sample size. A. sylvaticus Results of GLM indicated that PC1 was not significantly related to any of the independent factors examined (Table 3; likelihood test # 2 5 ¼ 5:1312, P=0.4001). The insignificant results had low power (<0.10) and it is possible that they are due to small sample size. Discussion We found that skull size in the three species examined here did not change temporally during the study period nor in relation to latitude. The same was true for body mass and body length of M. agrestis, the only species for which we had sufficient data on these parameters. Schmidt and Jensen (2003) showed that several species of Danish mammals underwent a change in their body length during the last 175 years, with the smaller ones generally increasing in size, and they attributed these changes to habitat fragmentation. Their sample included one of the species examined here (M. agrestis), but our data do not support their conclusion. Changes (probably temporal) in body size among populations of A. sylvaticus were reported in other studies. For example, Mikulová and Frynta (2001) found slight but statistically significant differences between samples from localities in Prague city
4 62 Acta Theriol (2012) 57:59 63 Table 1 Results of multiple regressions examining the effects of latitude, longitude, year and month on PC1 (n=182), body length (127) and body mass (121) of M. agrestis PC1 Body length Body mass Source df Estimate χ 2 P Estimate χ 2 P Estimate χ 2 P Intercept Longitude Latitude Month Year Sex Significant results are italicised. PC1 is the first axis of a PCA that combines the four skull measurements (log transformed for normality) centre and those from the periphery, and attributed this phenomenon to urbanisation or isolation by built-up areas. During the last few decades, it has become evident that changes in body size may take place within a short period of time (Millien et al. 2006). Such changes were reported for many mammals (particularly carnivores, but also rodents) and birds, as well as for reptiles and amphibians (Yom-Tov and Geffen 2011). In their review, Yom-Tov and Geffen (2011) argued that almost any species may show a geographical variation in body size if the key predictor(s) that influences its size varies to a large extent across its range. Although common, a change in size is not a universal reaction to changes in the environment. Cases of studied animals whose body size did not change temporally over the last century are poorly reported (but see Yom-Tov et al and Meiri et al. 2009). This bias in publication is due to authors, and particularly editors, being reluctant to publish negative results. Because such bias may consequently distort our understanding of biological processes in nature, it is important that these negative results also be published. In time, a larger body of knowledge on a more diverse selection of animals may provide a basis for a better understanding of the different organisms' reactions to the environment. Our results indicate that PC1, body size and body mass of M. agrestis increases from west to east. This may be interpreted as conforming to Bergmann's rule, which predicts that body size of warm-blooded animals will be negatively related to ambient temperature (Mayr 1970). Across northern Europe, ambient temperature decreases from west to east. A preliminary examination of global temperature data revealed that across latitude 55 N which passes through Denmark, and between 11 E and 14 E at 0.5 intervals, mean annual ambient temperature decreases significantly at a rate of 0.29 C per latitudinal degree (data downloaded from Potsdam Institute of Climate Impact Research; annual temperature= latitude; R 2 = , p=0.0222). Hence, body size of the vole in Denmark conforms to Bergmann's rule. We found that voles attain their maximal size (PC1, body length and body mass) during summer (Fig. 2). These results are most probably due to the availability of plentiful food during the Danish summer and that young voles attain their final body size in that period. Table 2 Results of multiple regressions examining the effects of latitude, longitude, year and month on PC1 of A. flavicollis (n=270) Source df Estimate χ 2 P Intercept Longitude Latitude Month Year Sex PC1 is the first axis of a PCA that combines the four skull measurements (log transformed for normality). The significant result is italicised Table 3 Results of multiple regressions examining the effects of latitude, longitude, year and month on PC1 of A. sylvaticus (n=178) Source df Estimate χ 2 P Intercept Longitude Latitude Month Year Sex PC1 is the first axis of a PCA that combines the four skull measurements (log transformed for normality)
5 Acta Theriol (2012) 57: Acknowledgements Shlomith and Yoram Yom-Tov wish to thank Mogens Andersen for his most efficient and kind help during their stay in Copenhagen and later on. The staff of the Zoological Museum of Copenhagen and COBICE were kind and efficient hosts to YYT and SYT. We thank Eli Geffen for his statistical advice and Naomi Paz for editorial advice and to two anonymous reviewers for their constructive comments. Work in Copenhagen was supported by a grant from the European Commission's programme Transnational Access to Major Research Infrastructures to COBICE (Copenhagen Biosystematics Center). References Alcantara M (1991) Geographic variation in body size of the wood mouse Apodemus sylvaticus. Mamm Rev 21: Gosler AG, Greenwood JJD, Perrins CM (1995) Predation risk and the cost of being fat. Nature 377: Lindstrom J (1999) Early development and fitness in birds and mammals. Tren Ecol Evol 14: Macdonald DW, Barrett P (1993) Mammals of Britain and Europe. HarperCollins, London Macdonald DW, Tattersall FT (2001) Britain's mammals the challenge for conservation. The Wildlife Conservation Research Unit, Oxford University Mayr E (1970) Population, species and evolution. Harvard University Press, Cambridge McNab KB (2010) Geographic and temporal correlations of mammalian size reconsidered: a resource rule. Oecologia 164:13 23 Meiri S, Guy D, Dayan T, Simberloff D (2009) Global change and carnivore body size: data are stasis. Glob Ecol Biog 18: Mikulová P, Frynta D (2001) Test of character displacement in urban populations of Apodemus sylvaticus. Canad J Zool 79: Millien V, Lyons SK, Olson L, Smith FA, Wilson AB, Yom-Tov Y (2006) Ecotypic variation in the context of global climate change: revisiting the rules. Ecol Lett 9: Pergams ORW, Ashley MV (2001) Microevolution in island rodents. Genetica : Schmidt NM, Jensen PM (2003) Changes in mammalian body length over 175 years adaptations to a fragmented landscape? Conser Ecol 7:6, Smith FA, Browning H, Shepherd UL (1998) The influence of climate change on the body mass of woodrats Neotoma in arid region of New Mexico, USA. Ecography 21: Wójcik AM, Polly PD, Sikorski MD, Wójcik JM (2006) Selection in a cycling population: differential response among skeletal traits. Evolution 60: Yom-Tov Y, Geffen E (2011) Recent spatial and temporal changes in body size of terrestrial vertebrates: probable causes and pitfalls. Biol Rev 86: Yom-Tov Y, Green W, Coleman J (1986) Morphological changes in the brush-tail possum in New Zealand. J Zool London 208: Yom-Tov Y, Yom-Tov S, Baagøe H (2003) Increase of skull size in the red fox (Vulpes vulpes) and Eurasian badger (Meles meles) in Denmark during the twentieth century: an effect of improved diet? Evol Ecol Res 5: Yom-Tov Y, Yom-Tov S, Wright J, Thorne CJR, Du Feu R (2006) Recent changes in body weight and wing length among some British passerine birds. Oikos 112: Yom-Tov Y, Leader N, Yom-Tov S, Baagøe HJ (2010) Temperature trends and recent decline in body size of the stone marten Martes foina in Denmark. Mamm Biol 75:
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