Oecologia DOI 10.1007/s00442-015-3340-4
POPULATION ECOLOGY - ORIGINAL RESEARCH
Rethinking biogeographic patterns: high local variation in relation to latitudinal clines for a widely distributed species Melissa R. Tesche1 · Karen E. Hodges1
Received: 9 September 2014 / Accepted: 3 May 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract Wide-ranging species typically differ morphologically across their ranges. Bergmann’s rule suggests that taxa in colder environments are bigger than related taxa in warmer locations. We examined 767 painted turtles (Chrysemys picta) in ten populations near their northwestern range edge in south-central British Columbia, Canada, in conjunction with previous data, to test the hypotheses of (1) a Bergmann’s latitudinal cline, and (2) that males and females show similar latitudinal variation in size. We also explicitly test the impact of high local variation on rangewide inference. Female and male turtles showed similar latitudinal clines in body size; the degree of sexual dimorphism did not change across the range. Importantly, local variation in sexual dimorphism across ponds was nearly as high as the previously observed continental variation. Indeed, we found both the lowest and the highest degrees of sexual size dimorphism that have ever been reported for this species. Further, differing criteria in the literature for identifying mature females compound the difficulty of interpreting latitudinal clines in size or dimorphism. Our results highlight the need for much more systematic local and regional sampling as inputs for latitudinal or other comparative analyses such as Rensch’s rule because insufficient sampling of high local variation may mask important ecological and evolutionary patterns.
Communicated by Lin Schwarzkopf. * Karen E. Hodges [email protected] 1
Department of Biology, University of British Columbia Okanagan, Science Building, 1177 Research Road, Kelowna, BC V1V 1V7, Canada
Keywords Bergmann’s rule · Painted turtle · Size dimorphism · Chrysemys picta · Rensch’s rule
Introduction The formation and investigation of biogeographic rules are popular, but contentious, pursuits (Geist 1987; Blackburn et al. 1999; Ashton 2001). Bergmann’s rule, originally proposed in 1847 to describe a negative relationship between temperature and body size in endotherms (Mayr 1956), is still debated. Latitude is often used as a proxy for temperature, and current investigations of Bergmann’s rule usually centre around detecting the trend or converse trend in different taxonomic groups and trying to infer possible mechanisms behind the observed patterns. For ectotherms, researchers are still identifying the major patterns in body size in relation to latitudinal or temperature gradients, let alone developing adaptive explanations for such patterns (Meiri 2011). Recent research investigates trends in body size in amphibians (Olalla-Tárraga and Rodríguez 2007; Adams and Church 2008), fish (Rypel 2014), insects and other arthropods (Blanckenhorn and Demont 2004; Eweleit and Reinhold 2014; Hassall et al. 2014), and reptiles (Ashton and Feldman 2003; Pincheira-Donoso and Meiri 2013). For example, Ashton and Feldman (2003) found that squamate reptiles appear to follow reverse Bergmann’s clines (with smaller individuals at more northerly latitudes), whereas 19 of 23 species of Chelonians had Bergmann’s clines. More recent work on squamates confirms they seldom exhibit Bergmann’s clines (Pincheira-Donoso et al. 2008; Pincheira-Donoso and Meiri 2013). For freshwater fish in North America, cool- and cold-water species showed Bergmann’s clines, whereas warm-water species
13
Oecologia
displayed reversed clines (Rypel 2014). In every ectothermic taxon examined so far, some species do not appear to show latitudinal clines in either direction. Various explanations have been floated for the different patterns, starting with the original explanation of heat conservation that Bergmann gave for endotherms: larger animals have lower surface area to volume ratios and hence animals in northern/cooler areas could conserve heat more effectively if they were larger. As Aragón and Fitze (2014) outline, ectothermic Bergmann’s clines could arise due to longer maturation times leading to larger sizes at maturation and reverse Bergmann’s clines in ectotherms could arise because small ectotherms absorb environmental heat faster than large ones. They also indicate that seasonality and resource abundance could affect body sizes, such that detecting latitudinal or other spatial patterns in temperature, precipitation, and resources could predict local body masses. Although turtles are ectothermic, a heat-conservation hypothesis has been suggested to explain their Bergmann’s clines. Larger body size, in combination with the thermal properties of the shell, may help turtles maintain elevated body temperatures for longer (Litzgus and Brooks 1998; Ashton and Feldman 2003). This hypothesis would be congruent with the observed reverse Bergmann trend observed in squamate reptiles, which lack the extra thermodynamic protection of a shell. Further, because most turtles are semiaquatic or aquatic, the thermal environments they inhabit are quite different in terms of seasonal and diurnal temperature variation than is the case for terrestrial squamates, suggesting different body size patterns may arise from these different environments. A second proposed mechanism behind the chelonian size trends relates to the physiological demands of increasingly harsh overwintering periods of northern habitats (Brooks et al. 1992). Larger turtles can accumulate greater energy stores and could be better equipped to deal with the longer periods of food shortage and decreased habitat productivity that come with the seasonality of northern latitudes (Ashton and Feldman 2003).
Body Size
(a)
In sexually dimorphic taxa, where one sex is consistently larger than the other, clinal variation in body size may differ for males and females, so tests of Bergmann’s rule need to evaluate males and females separately. Sexual size dimorphism arises as a result of different selective pressures (Berry and Shine 1980), with three main adaptive explanations (Stephens and Wiens 2009): sexual selection that favours larger males, fecundity selection that favours larger females, and ecological divergence of the sexes because of intraspecific competition, which could explain either sex being larger. If male and female body sizes change similarly with latitude, their slopes would be parallel and the degree of dimorphism would remain constant (Fig. 1a). If females have a steeper cline (Fig. 1b), male and female sizes would diverge and dimorphism would increase with latitude. If males have a steeper cline (Fig. 1c), male and female sizes would converge and dimorphism would decrease with latitude. Assessing which pattern occurs with latitude thus offers critical evolutionary insights, but doing so is complicated by the fact that estimating sexual size dimorphism can suffer: (1) when local variation in body sizes is large, (2) from sampling biases, or (3) from improper estimates of maturity. If local populations are highly variable in body sizes of either or both sexes, latitudinal or other large geographical patterns could be falsely inferred if local variation is insufficiently sampled. Biases can arise if traps preferentially catch one sex or certain sizes of animal (Tesche and Hodges 2015), or if museums prefer large specimens. Maturity threshold values are particularly important in species where it is difficult to distinguish between the sexes or to identify sexual maturity, both of which may occur for reptile species with temperature-dependent sex determination. The preferred index of sexual size dimorphism considers only mature adults (Lovich and Gibbons 1992); the threshold size at which an animal is considered a mature adult is thus inherently important, as the inclusion of smaller individuals will bias the estimated mean body size towards a lower value.
(b)
F
F M
M
(c)
F M
Latitude Fig. 1 Possible Bergmann’s clines for males (M) and females (F) when females are the larger sex. If both sexes respond similarly to latitude (a), the clines will be parallel and dimorphism will be constant.
13
If female body size has a steeper cline (b), dimorphism will increase with latitude. If male body size has a steeper cline (c), dimorphism will decrease with latitude. Adapted from Blanckenhorn et al. (2006)
Oecologia
The painted turtle, Chrysemys picta, is an excellent model for investigating geographic clines in body size because it is relatively common and has an extensive range across North America. Chrysemys has female-biased sexual dimorphism, with females reaching much larger sizes than males. The genus is well studied throughout the range, and a variety of life history information is available for populations across the US and Canada. Moll (1973) compared data from five eastern states and found a north–south cline, with age and minimum size at maturity smallest in Louisiana populations (Chrysemys picta dorsalis) and greatest in Wisconsin populations (Chrysemys picta bellii). Larger and more recent studies also found that painted turtles follow Bergmann’s rule (Ashton and Feldman 2003; Lindeman 1997), although these studies were missing body size data from the northwestern portion of the range. Based on limited data, northern painted turtles appear to mature later and at bigger sizes, and have larger clutches and lower clutch frequencies than southern conspecifics (Christiansen and Moll 1973; Iverson and Smith 1993; St. Clair et al. 1994). These patterns suggest that northern females are under selective pressure to increase body size in order to increase fecundity (Litzgus and Smith 2010). Males would not face this pressure, so potentially the latitudinal cline in female body size should be steeper than that of the males, and the dimorphism should increase with latitude. Litzgus and Smith (2010) found the opposite trend, however, showing a weak and slight negative relationship between latitude and dimorphism in painted turtles. Litzgus and Smith (2010) also cited the need for body size data from the northwestern range edge. Previous analyses of Bergmann’s trend or sexual dimorphism in painted turtles have relied on museum specimens or samples from single ponds, often with very low numbers of turtles (as few as one male:one female) used to represent each locality (Ashton and Feldman 2003; Litzgus and Smith 2010). Local conditions, like ambient air temperatures (Brooks et al. 1992), elevation (Cooley et al. 2003), and habitat productivity (Brown et al. 1994) are potentially important sources of variation in the life history traits of turtles. If body size of painted turtles varies substantially within or between ponds in a local area, this limited sampling may have given rise to spurious biogeographic patterns. Our work in British Columbia (BC), Canada provides these much-needed data from the northwestern range edge of painted turtles. More importantly, we also assess how much local variation in body size occurs across multiple ponds in the region. We examine average body size and degree of dimorphism for ten populations of painted turtles in southcentral BC, and compare these data to previous data from throughout the range. Our objectives were to:
1. Estimate local variability in painted turtle body size and sexual dimorphism in their northwestern range edge. 2. Examine whether Bergmann’s clines and latitudinal clines in sexual dimorphism are supported when these data from a previously unknown part of the range are included. 3. Compare local variation to the previously observed latitudinal variation to explore whether previous biogeographic inferences based on much smaller and more localized sample sizes should be revisited.
Materials and methods Four subspecies of painted turtle are recognized (Ernst and Lovich 2009), but the genus is undergoing taxonomic revision due to recent genetic work that potentially elevates Chrysemys picta dorsalis to species status [as C. dorsalis (Crother 2012; Jensen et al. 2014a)]. For convenience in this paper, we refer to subspecies, but we acknowledge the unresolved taxonomy. All subspecies, including C. picta dorsalis, interbreed along their range edges, and variation in life history traits is more tied to local conditions than to subspecific status (Lindeman 1997). Field sampling in BC Fieldwork was conducted in the Okanagan Valley of southcentral BC, Canada, between May and September 2009. The Okanagan Valley is a part of the northern range edge for painted turtles. The region is semi-arid, with large lakes on the valley bottom bordered by low-sloped hills of open canopy ponderosa pine (Pinus ponderosa) forests, shrubsteppe habitat dominated by big sagebrush (Artemisia tridentata), and grasslands. We surveyed turtles at ten ponds throughout the central and southern valley. The elevations of ponds ranged from 385 m on the valley bottom to 924 m and ponds were selected to represent the range of rural– urban settings in which turtle populations are found in this region (Tesche and Hodges 2015). Each pond was trapped for a single capture-mark-recapture session of 3–8 sunny days. The length of each trapping session was determined by the recapture rate, as we trapped for a longer period at sites with low recapture rates in an attempt to improve population estimates (Tesche and Hodges 2015). Three hoop nets (76.2 cm diameter, 3.81 cm2 mesh; Memphis Net and Twine, TN) were set at each pond. Hoop nets were secured with steel posts in the vegetated shallows of the ponds and baited by dangling a pierced can of cat food inside the middle hoop. Three basking traps (Sun Deck Turtle Trap; Heinson’s Country Store, TX) were also set at each pond. The traps were made of
13
Oecologia Table 1 Data sources used in the analysis of clinal variation in body size and sexual size dimorphism in Chrysemys picta
State/province
Study location
Louisiana
31°26′N, 91°38′W
21
37
Moll (1973)
New Mexico
35°5′N, 106°37′W
55
54
Christiansen and Moll (1973)
Tennessee
36°21′N, 89°9′W
17
19
Moll (1973)
Colorado
37°20′N, 107°52′W
57
38
Cooley et al. (2003)
Virginia
37°32′N, 77°28′W
1224
735
Illinois
39°31′N, 88°31′W
55
45
Moll (1973)
Pennsylvania
40°2′N, 76°15′W
30
50
Ernst (1971)
Minnesota
44°20′N, 94°15′W
32
23
Legler (1954)
Wisconsin
46°42′N, 90°33′W
32
23
Moll (1973)
Washington
46°45′N, 116°56′W
78
36
Lindeman (1996)
Wisconsin
46°71′N, 90°56′W
32
28
Christiansen and Moll (1973)
Idaho
47°27′N, 117°34′W
57
22
Lindeman (1996)
Saskatchewan
49°37′N, 103°48′W
12
7
MacCulloch and Secoy (1983)
Saskatchewan
50°34′N, 104°52′W
64
61
MacCulloch and Secoy (1983)
British Columbia
49°24′N, 119°33′W
271
496
wire ramps attached to a floating polyvinyl chloride frame with a submerged wire basket that was also baited with cat food. Basking traps were secured at areas of the pond where we observed basking turtles. We also used fish landing nets from shore or canoe to scoop turtles from the open water or mud for 1.5 h in the morning of each trapping day. Turtles were uniquely marked by using a Dremel rotary tool and the shell filing system set out in Cagle (1939). Plastron length was measured using digital calipers and was used in all analyses as the index of body size. Turtles were considered to be mature males if they showed well-developed secondary sex characteristics (Frazer et al. 1993), including noticeably elongated foreclaws and a lengthened pre-cloacal tail region, with the cloaca located beyond the edge of the carapace. Field identification of mature females is difficult and is usually based on the absence of male secondary sex characteristics in combination with a size threshold. The threshold value used to determine female maturity varies widely between studies, from plastron lengths of 97 mm (Mitchell 1988) to 165 mm (Cooley et al. 2003). To assess the importance of this decision criterion for the biogeographic analyses, we used two different criteria when we classified fieldcaught turtles as adult females. First, we followed Griffin (2007), who considered turtles in northern Montana to be adult females if their plastron lengths exceeded 105 mm and they lacked secondary sex characteristics. This classification almost certainly excludes any males, since males would have secondary sexual characteristics at this size, but it could include some immature females since females may mature at bigger sizes than males. Second, we used a threshold plastron size based on work by St. Clair et al. (1994) in southeastern BC, who determined the smallest size of gravid turtles in their study population to be
13
n (males)
n (females)
References
Mitchell (1988)
This study
151 mm. This threshold is far less likely to contain immature turtles but could exclude some small mature females. We refer to these two criteria as “all females” and “mature females.” Biogeographic analysis We surveyed published literature for papers containing plastron-length data for populations of painted turtles. We included data only if the authors provided the mean plastron length for adult male and adult female turtles, with at least seven turtles total sampled in the population (Table 1). We set the inclusion threshold to seven because that was the fewest total turtles caught in the ponds we sampled, but the actual sample sizes of populations from the literature ranged from 19 to 1959 adult turtles. Mean sample size ± SE (median) was 126 ± 85 (44) for males, and 84 ± 50 (37) for females. The data represent painted turtle populations in 12 states and provinces, ranging from 31–50°N and 76–119°W. We calculated the sexual size dimorphism index as (mean female size/mean male size), as recommended by Lovich and Gibbons (1992). We used linear regression to test for relationships between latitude and male size, female size, and the sexual size dimorphism index.
Results Local variation in size of painted turtles In ten ponds in southcentral BC, we captured 7–322 turtles per pond. Of these turtles, 271 male turtles had well-defined secondary sex characteristics. We caught 496 turtles with
Oecologia
Biogeographic patterns in body size Plastron lengths for males and females had similar positive linear relationships with latitude (Fig. 2a). There was a very weak and non-significant negative linear relationship between the sexual dimorphism index and latitude (Fig. 2b). The local variation in plastron length of painted turtles in BC spanned 20–30 % of the variation observed from across the rest of the geographic range. Male means across the range varied from 73 to 174 mm, while local variation ranged from 112 to 133 mm (Fig. 3); for females, rangewide variation was 114–202 mm and BC values for mature females were 157–181 mm (Fig. 4). Dimorphism indices for the BC populations had very high variation between ponds (Fig. 5). Indeed, local variation in the dimorphism index for the Okanagan valley encompassed most of the geographic variation across the range. Range-wide dimorphism varied from 1.15 to 1.56, whereas dimorphism in ten BC ponds for mature females ranged from 1.27 to 1.61. When using the plastron length of mature females, one of the Okanagan populations had the highest degree of dimorphism recorded in North America (1.61); when using the index calculated with all females, one of the Okanagan populations had the lowest degree of dimorphism recorded (1.15). Substantial local variation also occurred in three other jurisdictions where more than one pond was sampled: Colorado, Wisconsin, and particularly, Saskatchewan. For male turtles, the size of the smallest individuals with secondary sex characteristics varied significantly with latitude (Fig. 6). The size of the smallest males ranged from 60 to 129 mm across the range. In the BC ponds sampled, the smallest males we recorded per pond averaged 80.1 mm (range 64.9–94.9 mm). For females, researchers used a range
Plastron Length (mm)
(a)
210 190 170 150 130 110 90 70 50
(b) Sexual Dimorphism Index
plastron lengths >105 mm and lacking secondary sexual characteristics; these turtles were classified as female. Of these female turtles, 289 had plastron lengths >151 mm and were considered as mature females. Across all adult turtles, the mean plastron length was 121.8 ± 2.4 mm for males (median 119.9), 151.5 ± 2.7 mm for all females (median 152.8), and 170.5 ± 2.2 mm for mature females (median 171.1). The mean male plastron length was significantly smaller than both the mean plastron length of all females (t = 10.92, p
POPULATION ECOLOGY - ORIGINAL RESEARCH
Rethinking biogeographic patterns: high local variation in relation to latitudinal clines for a widely distributed species Melissa R. Tesche1 · Karen E. Hodges1
Received: 9 September 2014 / Accepted: 3 May 2015 © Springer-Verlag Berlin Heidelberg 2015
Abstract Wide-ranging species typically differ morphologically across their ranges. Bergmann’s rule suggests that taxa in colder environments are bigger than related taxa in warmer locations. We examined 767 painted turtles (Chrysemys picta) in ten populations near their northwestern range edge in south-central British Columbia, Canada, in conjunction with previous data, to test the hypotheses of (1) a Bergmann’s latitudinal cline, and (2) that males and females show similar latitudinal variation in size. We also explicitly test the impact of high local variation on rangewide inference. Female and male turtles showed similar latitudinal clines in body size; the degree of sexual dimorphism did not change across the range. Importantly, local variation in sexual dimorphism across ponds was nearly as high as the previously observed continental variation. Indeed, we found both the lowest and the highest degrees of sexual size dimorphism that have ever been reported for this species. Further, differing criteria in the literature for identifying mature females compound the difficulty of interpreting latitudinal clines in size or dimorphism. Our results highlight the need for much more systematic local and regional sampling as inputs for latitudinal or other comparative analyses such as Rensch’s rule because insufficient sampling of high local variation may mask important ecological and evolutionary patterns.
Communicated by Lin Schwarzkopf. * Karen E. Hodges [email protected] 1
Department of Biology, University of British Columbia Okanagan, Science Building, 1177 Research Road, Kelowna, BC V1V 1V7, Canada
Keywords Bergmann’s rule · Painted turtle · Size dimorphism · Chrysemys picta · Rensch’s rule
Introduction The formation and investigation of biogeographic rules are popular, but contentious, pursuits (Geist 1987; Blackburn et al. 1999; Ashton 2001). Bergmann’s rule, originally proposed in 1847 to describe a negative relationship between temperature and body size in endotherms (Mayr 1956), is still debated. Latitude is often used as a proxy for temperature, and current investigations of Bergmann’s rule usually centre around detecting the trend or converse trend in different taxonomic groups and trying to infer possible mechanisms behind the observed patterns. For ectotherms, researchers are still identifying the major patterns in body size in relation to latitudinal or temperature gradients, let alone developing adaptive explanations for such patterns (Meiri 2011). Recent research investigates trends in body size in amphibians (Olalla-Tárraga and Rodríguez 2007; Adams and Church 2008), fish (Rypel 2014), insects and other arthropods (Blanckenhorn and Demont 2004; Eweleit and Reinhold 2014; Hassall et al. 2014), and reptiles (Ashton and Feldman 2003; Pincheira-Donoso and Meiri 2013). For example, Ashton and Feldman (2003) found that squamate reptiles appear to follow reverse Bergmann’s clines (with smaller individuals at more northerly latitudes), whereas 19 of 23 species of Chelonians had Bergmann’s clines. More recent work on squamates confirms they seldom exhibit Bergmann’s clines (Pincheira-Donoso et al. 2008; Pincheira-Donoso and Meiri 2013). For freshwater fish in North America, cool- and cold-water species showed Bergmann’s clines, whereas warm-water species
13
Oecologia
displayed reversed clines (Rypel 2014). In every ectothermic taxon examined so far, some species do not appear to show latitudinal clines in either direction. Various explanations have been floated for the different patterns, starting with the original explanation of heat conservation that Bergmann gave for endotherms: larger animals have lower surface area to volume ratios and hence animals in northern/cooler areas could conserve heat more effectively if they were larger. As Aragón and Fitze (2014) outline, ectothermic Bergmann’s clines could arise due to longer maturation times leading to larger sizes at maturation and reverse Bergmann’s clines in ectotherms could arise because small ectotherms absorb environmental heat faster than large ones. They also indicate that seasonality and resource abundance could affect body sizes, such that detecting latitudinal or other spatial patterns in temperature, precipitation, and resources could predict local body masses. Although turtles are ectothermic, a heat-conservation hypothesis has been suggested to explain their Bergmann’s clines. Larger body size, in combination with the thermal properties of the shell, may help turtles maintain elevated body temperatures for longer (Litzgus and Brooks 1998; Ashton and Feldman 2003). This hypothesis would be congruent with the observed reverse Bergmann trend observed in squamate reptiles, which lack the extra thermodynamic protection of a shell. Further, because most turtles are semiaquatic or aquatic, the thermal environments they inhabit are quite different in terms of seasonal and diurnal temperature variation than is the case for terrestrial squamates, suggesting different body size patterns may arise from these different environments. A second proposed mechanism behind the chelonian size trends relates to the physiological demands of increasingly harsh overwintering periods of northern habitats (Brooks et al. 1992). Larger turtles can accumulate greater energy stores and could be better equipped to deal with the longer periods of food shortage and decreased habitat productivity that come with the seasonality of northern latitudes (Ashton and Feldman 2003).
Body Size
(a)
In sexually dimorphic taxa, where one sex is consistently larger than the other, clinal variation in body size may differ for males and females, so tests of Bergmann’s rule need to evaluate males and females separately. Sexual size dimorphism arises as a result of different selective pressures (Berry and Shine 1980), with three main adaptive explanations (Stephens and Wiens 2009): sexual selection that favours larger males, fecundity selection that favours larger females, and ecological divergence of the sexes because of intraspecific competition, which could explain either sex being larger. If male and female body sizes change similarly with latitude, their slopes would be parallel and the degree of dimorphism would remain constant (Fig. 1a). If females have a steeper cline (Fig. 1b), male and female sizes would diverge and dimorphism would increase with latitude. If males have a steeper cline (Fig. 1c), male and female sizes would converge and dimorphism would decrease with latitude. Assessing which pattern occurs with latitude thus offers critical evolutionary insights, but doing so is complicated by the fact that estimating sexual size dimorphism can suffer: (1) when local variation in body sizes is large, (2) from sampling biases, or (3) from improper estimates of maturity. If local populations are highly variable in body sizes of either or both sexes, latitudinal or other large geographical patterns could be falsely inferred if local variation is insufficiently sampled. Biases can arise if traps preferentially catch one sex or certain sizes of animal (Tesche and Hodges 2015), or if museums prefer large specimens. Maturity threshold values are particularly important in species where it is difficult to distinguish between the sexes or to identify sexual maturity, both of which may occur for reptile species with temperature-dependent sex determination. The preferred index of sexual size dimorphism considers only mature adults (Lovich and Gibbons 1992); the threshold size at which an animal is considered a mature adult is thus inherently important, as the inclusion of smaller individuals will bias the estimated mean body size towards a lower value.
(b)
F
F M
M
(c)
F M
Latitude Fig. 1 Possible Bergmann’s clines for males (M) and females (F) when females are the larger sex. If both sexes respond similarly to latitude (a), the clines will be parallel and dimorphism will be constant.
13
If female body size has a steeper cline (b), dimorphism will increase with latitude. If male body size has a steeper cline (c), dimorphism will decrease with latitude. Adapted from Blanckenhorn et al. (2006)
Oecologia
The painted turtle, Chrysemys picta, is an excellent model for investigating geographic clines in body size because it is relatively common and has an extensive range across North America. Chrysemys has female-biased sexual dimorphism, with females reaching much larger sizes than males. The genus is well studied throughout the range, and a variety of life history information is available for populations across the US and Canada. Moll (1973) compared data from five eastern states and found a north–south cline, with age and minimum size at maturity smallest in Louisiana populations (Chrysemys picta dorsalis) and greatest in Wisconsin populations (Chrysemys picta bellii). Larger and more recent studies also found that painted turtles follow Bergmann’s rule (Ashton and Feldman 2003; Lindeman 1997), although these studies were missing body size data from the northwestern portion of the range. Based on limited data, northern painted turtles appear to mature later and at bigger sizes, and have larger clutches and lower clutch frequencies than southern conspecifics (Christiansen and Moll 1973; Iverson and Smith 1993; St. Clair et al. 1994). These patterns suggest that northern females are under selective pressure to increase body size in order to increase fecundity (Litzgus and Smith 2010). Males would not face this pressure, so potentially the latitudinal cline in female body size should be steeper than that of the males, and the dimorphism should increase with latitude. Litzgus and Smith (2010) found the opposite trend, however, showing a weak and slight negative relationship between latitude and dimorphism in painted turtles. Litzgus and Smith (2010) also cited the need for body size data from the northwestern range edge. Previous analyses of Bergmann’s trend or sexual dimorphism in painted turtles have relied on museum specimens or samples from single ponds, often with very low numbers of turtles (as few as one male:one female) used to represent each locality (Ashton and Feldman 2003; Litzgus and Smith 2010). Local conditions, like ambient air temperatures (Brooks et al. 1992), elevation (Cooley et al. 2003), and habitat productivity (Brown et al. 1994) are potentially important sources of variation in the life history traits of turtles. If body size of painted turtles varies substantially within or between ponds in a local area, this limited sampling may have given rise to spurious biogeographic patterns. Our work in British Columbia (BC), Canada provides these much-needed data from the northwestern range edge of painted turtles. More importantly, we also assess how much local variation in body size occurs across multiple ponds in the region. We examine average body size and degree of dimorphism for ten populations of painted turtles in southcentral BC, and compare these data to previous data from throughout the range. Our objectives were to:
1. Estimate local variability in painted turtle body size and sexual dimorphism in their northwestern range edge. 2. Examine whether Bergmann’s clines and latitudinal clines in sexual dimorphism are supported when these data from a previously unknown part of the range are included. 3. Compare local variation to the previously observed latitudinal variation to explore whether previous biogeographic inferences based on much smaller and more localized sample sizes should be revisited.
Materials and methods Four subspecies of painted turtle are recognized (Ernst and Lovich 2009), but the genus is undergoing taxonomic revision due to recent genetic work that potentially elevates Chrysemys picta dorsalis to species status [as C. dorsalis (Crother 2012; Jensen et al. 2014a)]. For convenience in this paper, we refer to subspecies, but we acknowledge the unresolved taxonomy. All subspecies, including C. picta dorsalis, interbreed along their range edges, and variation in life history traits is more tied to local conditions than to subspecific status (Lindeman 1997). Field sampling in BC Fieldwork was conducted in the Okanagan Valley of southcentral BC, Canada, between May and September 2009. The Okanagan Valley is a part of the northern range edge for painted turtles. The region is semi-arid, with large lakes on the valley bottom bordered by low-sloped hills of open canopy ponderosa pine (Pinus ponderosa) forests, shrubsteppe habitat dominated by big sagebrush (Artemisia tridentata), and grasslands. We surveyed turtles at ten ponds throughout the central and southern valley. The elevations of ponds ranged from 385 m on the valley bottom to 924 m and ponds were selected to represent the range of rural– urban settings in which turtle populations are found in this region (Tesche and Hodges 2015). Each pond was trapped for a single capture-mark-recapture session of 3–8 sunny days. The length of each trapping session was determined by the recapture rate, as we trapped for a longer period at sites with low recapture rates in an attempt to improve population estimates (Tesche and Hodges 2015). Three hoop nets (76.2 cm diameter, 3.81 cm2 mesh; Memphis Net and Twine, TN) were set at each pond. Hoop nets were secured with steel posts in the vegetated shallows of the ponds and baited by dangling a pierced can of cat food inside the middle hoop. Three basking traps (Sun Deck Turtle Trap; Heinson’s Country Store, TX) were also set at each pond. The traps were made of
13
Oecologia Table 1 Data sources used in the analysis of clinal variation in body size and sexual size dimorphism in Chrysemys picta
State/province
Study location
Louisiana
31°26′N, 91°38′W
21
37
Moll (1973)
New Mexico
35°5′N, 106°37′W
55
54
Christiansen and Moll (1973)
Tennessee
36°21′N, 89°9′W
17
19
Moll (1973)
Colorado
37°20′N, 107°52′W
57
38
Cooley et al. (2003)
Virginia
37°32′N, 77°28′W
1224
735
Illinois
39°31′N, 88°31′W
55
45
Moll (1973)
Pennsylvania
40°2′N, 76°15′W
30
50
Ernst (1971)
Minnesota
44°20′N, 94°15′W
32
23
Legler (1954)
Wisconsin
46°42′N, 90°33′W
32
23
Moll (1973)
Washington
46°45′N, 116°56′W
78
36
Lindeman (1996)
Wisconsin
46°71′N, 90°56′W
32
28
Christiansen and Moll (1973)
Idaho
47°27′N, 117°34′W
57
22
Lindeman (1996)
Saskatchewan
49°37′N, 103°48′W
12
7
MacCulloch and Secoy (1983)
Saskatchewan
50°34′N, 104°52′W
64
61
MacCulloch and Secoy (1983)
British Columbia
49°24′N, 119°33′W
271
496
wire ramps attached to a floating polyvinyl chloride frame with a submerged wire basket that was also baited with cat food. Basking traps were secured at areas of the pond where we observed basking turtles. We also used fish landing nets from shore or canoe to scoop turtles from the open water or mud for 1.5 h in the morning of each trapping day. Turtles were uniquely marked by using a Dremel rotary tool and the shell filing system set out in Cagle (1939). Plastron length was measured using digital calipers and was used in all analyses as the index of body size. Turtles were considered to be mature males if they showed well-developed secondary sex characteristics (Frazer et al. 1993), including noticeably elongated foreclaws and a lengthened pre-cloacal tail region, with the cloaca located beyond the edge of the carapace. Field identification of mature females is difficult and is usually based on the absence of male secondary sex characteristics in combination with a size threshold. The threshold value used to determine female maturity varies widely between studies, from plastron lengths of 97 mm (Mitchell 1988) to 165 mm (Cooley et al. 2003). To assess the importance of this decision criterion for the biogeographic analyses, we used two different criteria when we classified fieldcaught turtles as adult females. First, we followed Griffin (2007), who considered turtles in northern Montana to be adult females if their plastron lengths exceeded 105 mm and they lacked secondary sex characteristics. This classification almost certainly excludes any males, since males would have secondary sexual characteristics at this size, but it could include some immature females since females may mature at bigger sizes than males. Second, we used a threshold plastron size based on work by St. Clair et al. (1994) in southeastern BC, who determined the smallest size of gravid turtles in their study population to be
13
n (males)
n (females)
References
Mitchell (1988)
This study
151 mm. This threshold is far less likely to contain immature turtles but could exclude some small mature females. We refer to these two criteria as “all females” and “mature females.” Biogeographic analysis We surveyed published literature for papers containing plastron-length data for populations of painted turtles. We included data only if the authors provided the mean plastron length for adult male and adult female turtles, with at least seven turtles total sampled in the population (Table 1). We set the inclusion threshold to seven because that was the fewest total turtles caught in the ponds we sampled, but the actual sample sizes of populations from the literature ranged from 19 to 1959 adult turtles. Mean sample size ± SE (median) was 126 ± 85 (44) for males, and 84 ± 50 (37) for females. The data represent painted turtle populations in 12 states and provinces, ranging from 31–50°N and 76–119°W. We calculated the sexual size dimorphism index as (mean female size/mean male size), as recommended by Lovich and Gibbons (1992). We used linear regression to test for relationships between latitude and male size, female size, and the sexual size dimorphism index.
Results Local variation in size of painted turtles In ten ponds in southcentral BC, we captured 7–322 turtles per pond. Of these turtles, 271 male turtles had well-defined secondary sex characteristics. We caught 496 turtles with
Oecologia
Biogeographic patterns in body size Plastron lengths for males and females had similar positive linear relationships with latitude (Fig. 2a). There was a very weak and non-significant negative linear relationship between the sexual dimorphism index and latitude (Fig. 2b). The local variation in plastron length of painted turtles in BC spanned 20–30 % of the variation observed from across the rest of the geographic range. Male means across the range varied from 73 to 174 mm, while local variation ranged from 112 to 133 mm (Fig. 3); for females, rangewide variation was 114–202 mm and BC values for mature females were 157–181 mm (Fig. 4). Dimorphism indices for the BC populations had very high variation between ponds (Fig. 5). Indeed, local variation in the dimorphism index for the Okanagan valley encompassed most of the geographic variation across the range. Range-wide dimorphism varied from 1.15 to 1.56, whereas dimorphism in ten BC ponds for mature females ranged from 1.27 to 1.61. When using the plastron length of mature females, one of the Okanagan populations had the highest degree of dimorphism recorded in North America (1.61); when using the index calculated with all females, one of the Okanagan populations had the lowest degree of dimorphism recorded (1.15). Substantial local variation also occurred in three other jurisdictions where more than one pond was sampled: Colorado, Wisconsin, and particularly, Saskatchewan. For male turtles, the size of the smallest individuals with secondary sex characteristics varied significantly with latitude (Fig. 6). The size of the smallest males ranged from 60 to 129 mm across the range. In the BC ponds sampled, the smallest males we recorded per pond averaged 80.1 mm (range 64.9–94.9 mm). For females, researchers used a range
Plastron Length (mm)
(a)
210 190 170 150 130 110 90 70 50
(b) Sexual Dimorphism Index
plastron lengths >105 mm and lacking secondary sexual characteristics; these turtles were classified as female. Of these female turtles, 289 had plastron lengths >151 mm and were considered as mature females. Across all adult turtles, the mean plastron length was 121.8 ± 2.4 mm for males (median 119.9), 151.5 ± 2.7 mm for all females (median 152.8), and 170.5 ± 2.2 mm for mature females (median 171.1). The mean male plastron length was significantly smaller than both the mean plastron length of all females (t = 10.92, p
