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Age and Body Size of Salamandrella Keyserlingii (Caudata: Hynobiidae): a Difference in Altitudes, Latitudes, and Temperatures

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Age and Body Size of Salamandrella Keyserlingii (Caudata: Hynobiidae): a Difference in Altitudes, Latitudes, and Temperatures Org Divers Evol (2012) 12:167–181 DOI 10.1007/s13127-012-0091-5 Age and body size of Salamandrella keyserlingii (Caudata: Hynobiidae): a difference in altitudes, latitudes, and temperatures Masato Hasumi & Leo J. Borkin Received: 20 December 2011 /Accepted: 23 April 2012 /Published online: 20 June 2012 # Gesellschaft für Biologische Systematik 2012 Abstract The debate surrounding Bergmann’s rule, in which Keywords Age structure . Bergmann’s rule . the body size of animals is predicted to be larger in cooler Ecogeography . Growth trajectory . Skeletochronology . environments, is still open concerning ectotherms. Our goal Terentjev’s optimum rule was to test this rule in the broadest ranging amphibian species Salamandrella keyserlingii. We determined age and body size in a cooler region (Darhadyn, Mongolia: mean yearly Introduction air temperature=–8.31 °C) using skeletochronology, and compared their differences in altitude, latitude, and tempera- Relationships between body size morphology and several ture with those of a warmer area (Kushiro, Japan: 7.98 °C). In key factors of climate, environment, and evolution poten- Darhadyn, both sexes reached sexual maturity at 5–6yearsof tially influence geographic patterns of body size variation of age (growth coefficient: male00.585, female00.266), organisms at ecological and evolutionary time scales (Mayr 2–3 years later than those in Kushiro (male01.341, female0 1965). Not only endotherms but also many ectotherms ma- 1.129). Mean body size was smaller in Darhadyn (53.08 mm) ture at larger size at lower rearing temperatures (Walters and than in Kushiro (57.63 mm) for males despite their constant Hassall 2006; Thomas 2009; Stillwell 2010). This has been metamorphic size around 30 mm. We also analyzed data termed the temperature–size rule, a pattern consistent with available from published studies for 27 populations within “Bergmann’s(1847)rule” (hereafter “Bergmann’srule”). the geographic range of this species from 43 to 69°N across Bergmann’s rule—a well-known ecogeographic pattern that a 2,900-km long latitudinal gradient. The analysis indicated an predicts larger body size with increasing latitude or decreas- intraspecific tendency to decrease body size with increased ing temperature—has received some degree of support in latitude from 43 to 57°N, to increase size from 57 to 69°N, most tetrapod groups [e.g., mammals, birds, chelonian rep- and to decrease body size with decreased temperature from 8 to tiles (turtles): Ashton 2004] and even in fish species –7 °C and increase size from –7to–15 °C. This pattern does (Thomas 2009). However, squamate reptiles (lizards and not follow the intraspecific extension of Bergmann’sruleand snakes) tend to decrease body size with high latitudes may follow the converse of Terentjev’s optimum rule—arule (Ashton and Feldman 2003). Geographic variation in body formulated to be an inverted-U shaped curve between size is complex in North American squamates, whereas increased latitude (or decreased temperature) and increased patterns in Europe are characterized by a clear latitudinal body size. decrease in body size (Olalla-Tárraga et al. 2006). Amphib- ians also seem to follow Bergmann’s rule (Ashton 2002), M. Hasumi (*) but Olalla-Tárraga and Rodríguez (2007) conducted an Biological Institute, Faculty of Science, Niigata University, assemblage-based analysis (for details see Olalla-Tárraga Niigata 950-2181, Japan e-mail: [email protected] et al. 2010) and revealed that, although anurans reach larger body size at colder climates in both Europe and North L. J. Borkin America, urodeles tend to be smaller in cooler areas. Adams Department of Herpetology, Zoological Institute, and Church (2008) analyzed a great number of museum Russian Academy of Sciences, Universitetskaya nab. 1, specimens of amphibians and concluded that, at the St. Petersburg 199034, Russian Federation intraspecific level, Bergmann’s rule does not apply to 168 M. Hasumi, L.J. Borkin amphibians: 3 of 40 species of the genus Plethodon follow portions of the body such as ears, limbs, and tail with high the rule, 7 show its converse, and 30 do not show any latitudes or low temperatures) is relatively unknown in ecto- geographic trend. The temperature–size rule, which predicts therms (Ray 1960). Furthermore, the optimum rule, originally a pattern consistent with Bergmann’s rule but relies on a formulated by Terentjev (1946, 1947, 1951, 1966), does not different mechanism, will help elucidate the application of seem to be known to the West, most likely because it is written Bergmann’s rule to ectotherms (Stillwell 2010). in Russian (hereafter called “Terentjev’soptimumrule”). He Bergmann’s rule, albeit originally defined as an interspecific agreed with Bergmann’s rule based on statistical analysis of pattern, was reformulated at the intraspecific level by Rensch intra- and inter-specific variation in body size of various ver- in 1938 (Blackburn et al. 1999). At the intraspecific level, tebrate species such as mammals, birds, snakes, and anurans. geographic variation in amphibian life-history traits, such as However, he predicted that regression of body size on ambient age and body size at sexual maturity or maximum longevity, temperature was not linear and instead followed an inverted-U occurs across altitudinal, latitudinal, and environmental gra- shaped curve: decreases in the initial ambient temperatures dients (Morrison and Hero 2003; Schäuble 2004; Laugen et al. corresponded to increased body size to some intermediate 2005). An altitudinal difference in age and body size is docu- maximum, after which decreases in the next ambient temper- mented in many European species (e.g., Miaud et al. 2000; atures corresponded to decreased body size. This pattern was Krizmanic et al. 2005;Amatetal.2010). For example, com- predicted for both endotherms and ectotherms. Terentjev pared to maximum longevities of populations exposed to alti- (1946, 1947, 1951, 1966) also cautioned against the use of tudinal gradients, Ichthyosaura (formerly Triturus or incomplete geographic datasets (i.e., data deficiency). That is, Mesotriton) alpestris reaches up to 20 years of age in highlands increased body size with decreased temperatures in one case butisalwayslessthan10yearsoldinlowlands(Miaudetal. (Bergmann’s rule) and decreased body size with decreased 2000). Krizmanic et al. (2005) found that body size increases temperatures in another case (converse of Bergmann’srule) with high altitudes for Ichthyosaura alpestris and Lissotriton might be each of two different (i.e., increased and decreased) (formerly Triturus) vulgaris but not for Triturus carnifex. parts of the same nonlinear model, while a suggested mecha- However, data on latitudinal differences in life-history traits nism of Terentjev’s optimum rule is still unknown. are limited to a few species with a wide distribution range (e.g., In the context of the temperature–size rule with intraspe- Bufo bufo: Hemelaar 1988; Cvetkovic et al. 2009; Rana tem- cific versions of Bergmann’s rule and Terentjev’s optimum poraria:Paloetal.2003;Laugenetal.2005; Limnodynastes rule, our specific research questions were as follows: (1) Is peronii and Limnodynastes tasmaniensis: Schäuble 2004; Tri- body size at metamorphosis or after sexual maturity larger in turus cristatus: Litvinchuk and Borkin 2009). a “northern, high altitudinal population” (NH: cooler area) Salamandrella keyserlingii Dybowski, 1870 has the than in a “southern, low altitudinal population” (SL: warmer broadest range of any amphibian species worldwide (~12 area)? (2) Is age at sexual maturity older for males and million km2 from 43 to 72°N), extending from eastern Europe females in NH than in SL? (3) Is maximum longevity through subarctic Siberia to Kamchatka Peninsula and Kurile greaterinNHthaninSL?(4)Inwhichlocationisthe Islands, including the northern portions of Kazakhstan, growth coefficient smaller, in NH or in SL? (5) How appli- Mongolia, China, North Korea, and Japan (Borkin et al. cable is the inverted-U shaped curve of Terentjev’s optimum 1984; Kuzmin 1994; Borkin 1999). This species is usually rule to latitude/temperature–body size interaction? Regard- found in lowlands, but in the mountain range near Khovsgol ing Allen’s(1877) rule, is tail length smaller in NH than in Lake, Mongolia, an individual with the largest snout–vent SL? To address these questions and to establish whether length (76 mm) was found at the highest altitude (2,250 m patterns of body size variation can be explained by a differ- elevation: Litvinov and Skuratov 1986). This observation has ence in age structure of a population, we generated data on long supported the idea that S. keyserlingii follows Bergmann’s “lines of arrested growth” (LAG) for age estimation by the rule at the intraspecific level across altitudinal gradients. How- use of skeletochronology, a method that can depict a growth ever, the recent collection of the largest female (80 mm) in trajectory of organisms without using nonindependent re- Ekaterinburg (0 Sverdlovsk in the former Soviet Union: 280 m capture data (for details see Hasumi 2010), in S. keyserlin- elevation) challenges this idea (Vershinin 2007;V.L. gii. We then compared age structure and body size Vershinin, unpublished). Because of its wide distribution, morphology between a relatively northern, high-altitude detecting age and body size among populations from different (cool) population (Darhadyn, Mongolia: this study) and a parts of the species’ range could contribute to a better
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