Hofmeister et al 2013, Spatial variation in d15N of painted turtles

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Hofmeister et al 2013, Spatial variation in d15N of painted turtles
    NOTICE: WARNING CONCERNING COPYRIGHT RESTRICTIONS   The copyright law of the United States (Title 17, United States Code) governs the making of  photocopies or other reproductions of copyrighted material. Under certain conditions specified in the law, libraries and archives are authorized to furnish a  photocopy or other reproduction. One of these specific conditions is that the photocopy or reproduction is not to be "used for any purpose other than private study, scholarship, or research." If a user makes a request for, or later uses, a photocopy or reproduction for purposes in excess of "fair use," that user may be liable for copyright infringement. This institution reserves the right to refuse to accept a copying order if, in its judgment, fulfillment of the order would involve violation of copyright law.   ARTICLE Elevated levels of   15 N in riverine Painted Turtles( Chrysemys picta ): trophic enrichment or anthropogenic input? Natalie R. Hofmeister, Megan Welk, and Steven Freedberg  Abstract: The natural abundance of stable isotopes of elements in animal tissue is influenced by both biotic and abiotic factors.Biotically, animals feeding at higher trophic levels are enriched in the ratio of   15 N: 14 N (  15 N) relative to their food resources owingto the preferential excretion of   14 N. Abiotically, increases in   15 N may also reflect different sources of biologically availablenitrogen, including nitrogen resulting from denitrification of inorganic fertilizer. We studied variation in  15 N among fresh- water turtle populations to assess spatial variation in   15 N and to determine whether this variation can be attributed todifferences in nitrogen source or trophic enrichment. We examined nitrogen and carbon stable isotope ratios in duckweed(genus  Lemna  L.) and in Painted Turtles ( Chrysemys picta  (Schneider, 1783)) in aquatic ecosystems expected to be differentially affected by agricultural activity and denitrification of inorganic fertilizer. Across sites,  C. picta  15 N was strongly correlated with  Lemna   15 N and was elevated in sites influenced by agricultural activity. Furthermore, trophic position of turtles was notassociated with   15 N but was consistent with expected values for primary consumers in freshwater systems, indicating thatdifferences in tissue  15 N could be attributed to differences in initial sources of nitrogen in each ecosystem. Our results suggestthat care must be taken when attributing differences in isotopic values of animal populations to trophic factors.  Key words: Chrysemys picta , Painted Turtle, stable isotope, trophic position, nitrogen enrichment. Résumé :  L’abondance naturelle des isotopes stables d’éléments dans les tissus animaux est influencée par des facteurs tant biotiques qu’abiotiques. Sur le plan biotique, les animaux s’alimentant a` des niveaux trophiques élevés présentent des rapports 15 N: 14 N (  15 N) enrichis par rapport a` leurs ressources alimentaires en raison de l’excrétion préférentielle du  14 N. Sur le planabiotique, des augmentations du  15 N pourraient également refléter différentes sources d’azote biodisponible, dont de l’azoteproduit par la dénitrification d’engrais inorganiques. Nous avons étudié les variations du  15 N dans des populations de tortuesd’eau douce afin d’évaluer la variabilité spatiale de  15 N et de déterminer si cette variabilité peut être attribuée a` des différencesencequiconcernelessourcesd’azoteoul’enrichissementtrophique.Nousavonsexaminélesrapportsd’isotopesstablesd’azoteet de carbone dans des lentilles d’eau (genre  Lemna  L.) et des tortues peintes ( Chrysemys picta  (Schneider, 1783)) dans desécosystèmes aquatiques qui devraient présenter des incidences différentes de l’activité agricole et de la dénitrification d’engraisinorganiques. Pour l’ensemble des sites étudiés, les   15 N de  C. picta  étaient fortement corrélés aux   15 N de  Lemna  et étaientélevésdanslessitesinfluencésparl’activitéagricole.Enoutre,lapositiontrophiquedestortuesn’étaitpasassociéeau  15 N,maisconcordait avec les valeurs attendues pour des consommateurs primaires dans des systèmes dulcicoles, ce qui indique que les variations de  15 N dans les tissus pourraient être attribuables a` des différences en ce qui concerne les sources initiales d’azotedans chaque écosystème. Nos résultats semblent indiquer que la prudence est de mise dans l’attribution a` des facteurs tro-phiques des variations des valeurs isotopiques au sein de populations animales. [Traduit par la Rédaction]  Mots-clés : Chrysemys picta , tortue peinte, isotope stable, position trophique, enrichissement en azote. Introduction Stable isotope analysis has become a powerful tool for makinginferences about the diet of vertebrate animals. The isotopic com-position of an animal’s tissue is directly influenced by that of itsdiet (DeNiro and Epstein 1981; Gannes et al. 1997; West et al. 2006;  Wolf et al. 2009) and thus can be used to determine trophic posi-tion and nutrient source (Post 2002; Layman et al. 2007; Martínez del Rio et al. 2009). Nitrogen isotopes have been used to study trophic interactions in a wide range of animal systems (birds andmammals: Hobson et al. 1994; Kelly 2000; herpetofauna: Wallace et al. 2006; Seminoff et al. 2007; fish: Vander Zanden et al. 1997; Estrada et al. 2005), while the composition of isotopes of carboncanreflectdifferentsourcesofcarboninanimaldiets(DeNiroandEpstein 1978; Rubenstein and Hobson 2004). Isotopic fractionation is the process of differential incorpora-tion of isotopes of the same element into compounds during nat-ural processes. Although the  14 N isotope of nitrogen is moreabundantthan 15 N, 14 Nispreferentiallyexcretedbyheterotrophs,and thus tissue  15 N: 14 N ratios (expressed as  15 N) of consumers areelevated with respect to dietary   15 N (Minagawa and Wada 1984). This enrichment can be used to infer trophic level, such that  15 Nof consumers is consistently enriched by 2‰–4‰ relative to theirfood source (Minagawa and Wada 1984; Peterson and Fry 1987; Post 2002; Vanderklift and Ponsard 2003), although individual  variationintrophicshiftcancomplicatethepreciseestimationof trophic level (McCutchan et al. 2003). Thus, estimation of trophic position is a potentially valuable tool for explaining consumer  15 Nvariation,evenintheabsenceofanalysesofcommunityfood web dynamics. Received 23 May 2013. Accepted 24 October 2013. N.R. Hofmeister.  Department of Ecology, Evolution and Environmental Biology, Columbia University, 1200 Amsterdam Avenue, New York, NY 10027, USA. M. Welk.  College of Menominee Nation, Keshena, WI 54135, USA. S. Freedberg.  Department of Biology, St. Olaf College, 1520 St. Olaf Avenue, Northfield, MN 55057, USA. Corresponding author:  Steven Freedberg (e-mail: freedber@stolaf.edu). 899Can. J. Zool.  91 : 899–905 (2013) dx.doi.org/10.1139/cjz-2013-0121 Published at www.nrcresearchpress.com/cjz on 26 October 2013.    C  a  n .   J .   Z  o  o   l .   D  o  w  n   l  o  a   d  e   d   f  r  o  m  w  w  w .  n  r  c  r  e  s  e  a  r  c   h  p  r  e  s  s .  c  o  m   b  y   S   T   A   T   E   U   N   I   V   E   R   S   I   T   Y   N   Y  -   B   I   N   G   H   A   M   T   O   N  o  n   1   2   /   1   1   /   1   3   F  o  r  p  e  r  s  o  n  a   l  u  s  e  o  n   l  y .  Differences in the distribution of consumer  15 N among popu-lations of the same species often reflect intraspecific variation inmean trophic position among different ecosystems as a result of different feeding strategies ( Jennings et al. 1997; Fry 2002), but may also reflect variation in other traits related to isotopic signa-tures. For example, metabolism, which is partly under geneticcontrol, can influence isotope values of animals (Carleton andMartínez del Rio 2005; Pecquerie et al. 2010; Boecklen et al. 2011). Studying intraspecific genetic variation in stable isotope studiesmaythusofferadditionalinsightintopotentialsourcesofisotopic variation among animal populations. Variation in  15 N at the base of the food web may reflect differ-ences in the isotopic composition of primary producers. Differ-encesin  15 Nofprimaryproducerscancapturespatialvariationin basal  15 N (Post 2002), but primary consumer  15 N is often used asa baseline in stable isotope studies ( Vander Zanden and Rasmussen1999; Anderson and Cabana 2007). However, differences in base- line   15 N may not be conserved through multiple trophic levels( Wallace et al. 2006). In addition, use of primary producers for  baseline   15 N can control for differences in isotope turnover ordiscrimination between turtles (Seminoff et al. 2006; Reich et al. 2008; Rosenblatt and Heithaus 2013).  15 N of primary producers isexpectedtobeinfluencedbytheisotopiccompositionofnitrogensources. Both free-living and symbiotic micro-organisms fix ni-trogen, which is then incorporated by plants directly (as in root-nodule symbiosis) or as ammonium (Cleveland et al. 1999; Fry  2006). Anthropogenic input of nitrogen can significantly alter the iso-topic composition of biologically available nitrogen and subse-quently increase the   15 N of organisms in aquatic ecosystems(Cole et al. 2004; Anderson and Cabana 2005; Bannon and Roman 2008). This relationship is so consistent that comparisons of base-line   15 N among ecosystems have been used to infer anthro-pogenic nutrient input (Cabana and Rasmussen 1996; Kohzu et al. 2009). In particular, several studies report a direct correlation between nitrate concentration and isotopic composition of pri-mary producers in ecosystems influenced by human activity (Harrington et al. 1998; Lake et al. 2001). Inorganic fertilizer has  beenfoundtoincrease  15 Nlevelsinagriculturalsystemsthroughmicrobial denitrification, as denitrifying bacteria preferentially metabolize  14 N and cause enrichment of   15 N in the remainingnitrate (Mayer et al. 2002; Diebel and Vander Zanden 2009). Isotopic ratios of nitrogen vary among aquatic ecosystems dueto differences both in the biologically available nitrogen pool andin fractionation of this nitrogen by consumers ( Vander Zandenand Rasmussen 1999; Patoine et al. 2006; Di Lorenzo et al. 2012). Nitrogen loading in freshwater systems has significant implica-tions for   15 N levels, especially in agricultural systems. Becausedenitrification rates are greater in streams and rivers relative toponds and lakes (Richardson et al. 2004; Kreiling et al. 2011), higher primary producer   15 N is expected in rivers relative topopulations in standing water ( Jansson et al. 1994; Saunders and Kalff2001;Piña-OchoaandÁlvarez-Cobelas2006).Giventhatboth trophic position and sources of biologically available nitrogenmay cause variation in consumer  15 N among ecosystems, assess-ing the factors underlying spatial variation in consumer  15 N lev-els among aquatic ecosystems may be valuable in understandingstable isotopic variation in natural systems.Painted Turtles ( Chrysemys picta  (Schneider, 1783)) are omnivo-rousgeneralistswhosedietincludesalgae,vascularplants(includ-ingduckweed,genus  Lemna L.),aquaticinvertebrates,insects,and vertebratessuchasfishandfrogs(Ernstetal.1994). Chrysemys picta thrive in both river and pond ecosystems, and these differentecosystem types may be associated with different dietary habits, basal isotopic levels, or both. This study examined nitrogen andcarbon levels among five geographically distinct sites expected todiffer in the extent to which they are affected by agriculturalactivity. We also employed mitochondrial sequencing to controlfor the possible effects of intraspecific genetic differentiation onthe factors contributing to stable isotopic values. Intraspecific variation in both diet and ecosystem make  C. picta  ideal for study-ing the forces underlying   13 C and   15 N variation in vertebrateanimals. This work may shed light on how carbon and nitrogensource and enrichment affect stable isotopic composition inhigher vertebrates. Materials and methods  Trapping and processing Chrysemys picta  were trapped in five locations characterized by  varying levels of agricultural activity within the Mississippi wa-tershed in Minnesota, USA. “Northfield Pond” (44°27 = 52.96 == N,93°11 = 32.25 ==  W) and “Weaver Pond” (44°14 = 54.35 == N, 91°56 = 43.92 ==  W)are two pond systems in southern Minnesota in areas character-izedbyagriculturaluse.Bothofthesepondsystemsconsistoftwoponds separated by <0.7 km. “Weaver River” (44°16 = 23.67 == N,91°53 = 56.55 ==  W) and “Dakota River” (43°54 = 33.78 == N, 91°21 = 0.97 ==  W)are two sites in the Mississippi River in southern Minnesota adja-cent to areas characterized by heavy agricultural use. “PristineLake” is a lake free from agricultural impact in northern Minne-sota (47°58 = 6.91 == N, 91°50 = 0.86 ==  W). Two trap designs were used: baited hoop traps, which consisted of a seine with two hoop trapsoneachend,andfloatingbaskingtraps.Trapswerecheckedevery 24–48 h between June and July 2011 and 2012.For each turtle captured, we measured carapace and plastronlengthsandassignedauniquescutemarkforfutureidentificationprior to releasing the turtle. A tissue sample (a clipping of the tailtip) was collected and preserved in 95% ethanol for <2 months.  Lemna  sp. was present at all sites and is commonly consumed by  C. picta andtheirprey.Samplesof   Lemna sp.werecollectedfromatleast three different locations in each study site and were alsopreserved in 95% ethanol for <2 months. Short-term preservation(<6 months) shows a minimal effect on  15 N and  13 C (Sarakinoset al. 2002), especially with ethanol concentration between 80%–100%, although some uncertainty remains (Sweeting et al. 2004). Ethanol preservation did not significantly affect   15 N or   13 C inturtles (Barrow et al. 2008) or fish in freshwater aquatic systems (Syväranta et al. 2008). Stable isotope analysis Each  C. picta  tail tissue sample was finely diced with a blade by hand (Reich et al. 2008) and dried at 60 °C for at least 24 h, and a 0.2–0.7 mg sample was weighed and processed. Lipid extraction wasnotperformed,asthepercentlipidforemydidturtletailtissueis below the threshold suggested for lipid extraction or mathematicalnormalizationof   13 C(Pearsonetal.2013).Thisprocesswasrepeated  with the  Lemna  samples, which were weighed at 0.5–2 mg. Samples were run on an isotope-ratio mass spectrometer (Elemental Com- bustion System, Costech Instruments, model 4010 linked to aThermoscientific Delta V Mass Spectrometer) to test for isotopicnitrogen ( 15 N) and carbon ( 13 C) levels. We excluded one  13 C valuefrom all analyses because it was a statistical outlier. DNA sequencing DNA was extracted from the preserved tissue of three turtlesfrom each river site and Pristine Lake site and four turtles fromeach agricultural pond site using a Puregene DNA extraction kitfor cells and tissue (Gentra Corporation, Minneapolis, Minnesota, USA).A373bpmarkerforthemitochondrialregionwasamplifiedusingPCR(polymerasechainreaction)withprimersdevelopedby M. Sorenson at the University of Massachusetts (5 = -CAA GGG TGG ATC GGG CAT AAC-3 =  and 5 = -GTG CCT GAA AAA ACA ACC ACA GG-3 = ;Freedbergetal.2005).Thecyclingthermalparametersused were as follows: 1 cycle at 95 °C (4 min), followed by 40 cycles at95 °C (40 s), 55 °C (1 min), 72 °C (2 min), and a final cycle at 72 °C(8 min). Gel electrophoresis in a 2% agarose gel was used toconfirm amplification. Sequence analysis was performed on an 900 Can. J. Zool. Vol. 91, 2013Published by NRC Research Press    C  a  n .   J .   Z  o  o   l .   D  o  w  n   l  o  a   d  e   d   f  r  o  m  w  w  w .  n  r  c  r  e  s  e  a  r  c   h  p  r  e  s  s .  c  o  m   b  y   S   T   A   T   E   U   N   I   V   E   R   S   I   T   Y   N   Y  -   B   I   N   G   H   A   M   T   O   N  o  n   1   2   /   1   1   /   1   3   F  o  r  p  e  r  s  o  n  a   l  u  s  e  o  n   l  y .   ABI 3730 capillary sequencer. Sequences were aligned and ana-lyzed in Geneious version 4.5.5. Annotated sequences were depos-ited in GenBank. Statistical analysis Pairwise t  testswereusedtotestfordifferencesin  15 Nand  13 Camong turtles from the five collection sites, and for differences incarapace length between Weaver River and Weaver Pond turtles.Regression analysis was used to test the correlation between  Lemna  and  C. picta  15 N across sites. Trophic position for turtles ateach location was calculated using the method described by  Post(2002) with the formula:TP    1       15 N  C .  picta      15 N  Lemna  sp.    15 N    where the discrimination factor (  15 N) is 3.4. We tested for rela-tionships between carapace length and trophic position and car-apace length and  15 N at each site using regression analysis. Results Stable isotope analysis Stable isotope analysis of   C. picta  samples revealed that mean  15 N of turtles in each agricultural pond system was significantly lowerthan  15 Nofeitherriverinesite(  p <0.0001foreachcompar-ison; Table 1).  15 N of turtles from Pristine Lake was significantly lower (  p  < 0.0001) than  15 N of turtles from all other sites except Weaver Pond system (  p  = 0.31). There were no significant differ-encesin C. picta  15 Namongriversitesoramongagriculturalpondsites (  p  > 0.2 for all comparisons). Mean  Lemna   15 N of WeaverRiver and Dakota River turtles was significantly higher than allother sites (  p  < 0.02 for each comparison). Elevated  15 N levels in C. picta  were strongly correlated with mean  Lemna  15 N values foreach study site (  R  2 = 0.991,  p  = 0.00037; Fig. 1). There were no sex differences in  15 N at any site following Bonferroni correction formultiple comparisons.Mean   13 C of turtles in Pristine Lake was significantly higherthan  C. picta   13 C in every other site except Weaver River(  p  < 0.0004 for each comparison; Table 1). Mean   13 C of WeaverPondandRiverturtleswassignificantlyhigherthan  13 CofNorth-fieldPondandDakotaRiverturtles(  p <0.007forallcomparisons).Mean  Lemna  13 CinthePristineLakewassignificantlyhigherthanall other sites (  p  < 0.01 for each comparison). In addition, mean  Lemna   13 C in Dakota River was significantly higher than  Lemna  13 C in Weaver River (  p  = 0.011).  Trophic position Trophic position of Dakota River turtles was significantly lowerthan trophic position of Pristine Lake (  p  = 0.0081), Weaver Pond(  p  = 0.0007) and Northfield Pond (  p  = 0.0077) turtles, while trophicposition of Weaver River turtles was significantly lower than Weaver Pond turtles only (  p  = 0.0061; Fig. 2). There was no signif- icant relationship between mean  15 N and mean trophic positionamong sites (  R  2 = 0.01997,  p  = 0.254).Neither trophic position nor   15 N was significantly associated with turtle size among Weaver River, Dakota River, or PristineLakesites(  p >0.2).Withinagriculturalpondsystems,  15 Nbutnottrophic position is positively correlated with carapace length inNorthfield Pond (  p  = 0.010), while turtles at a higher trophic posi-tion were significantly larger in Weaver Pond (  p  = 0.0270). DNA sequencing  Aligned sequences were truncated to a fragment containing354 bp of clear, readable sequences. We found no evidence of among-site genetic differentiation, as all but one sample (fromDakota River) were identical for the same allele. Morphological comparisons Mean carapace length at each agricultural pond site was signif-icantly smaller than that of each riverine site (  p  < 0.0002 for allfour comparisons). Mean carapace length of turtles in PristineLake was significantly greater than that of turtles in each agricul-tural ponds (  p  < 0.0001), was marginally greater than that fromturtles in Weaver River (  p  = 0.053), and was not significantly dif-ferent from turtles from Dakota River (  p  = 0.587). Discussion  Variation in  15 N among tissue samples from animals is gener-ally attributed to either differences in trophic position or differ-ent sources of biologically available nitrogen in the ecosystem. Inthe present study, we found substantial variation in  15 N among C. picta  populations that was nearly perfectly correlated with  15 Nof primary producers (  R  2 = 0.99; Fig. 1). Among-site variation in primary producer  15 N is a strong indicator of different isotopiccomposition of nitrogen sources, suggesting that baseline   15 N values differ among sites and contribute to turtle isotopic values. Although higher trophic levels can also contribute to variation inconsumer  15 N, the sites with the highest  15 N values in our study  were characterized by the lowest trophic position, indicating thatdifferences in trophic position do not contribute to variation in  15 N among sites. We found significant differences in turtle   13 C between mostpairwise comparisons of populations (Fig. 3). Although intra- specificvariationin  13 Coffoodorganismscanleadtodifferencesinconsumer  13 C,variationin  13 Cisalsopredictedtocorrespondto different carbon sources (DeNiro and Epstein 1978; Tieszen et al. 1983). Thus, turtles at different sites may not feed on thesame primary producer sources. Interestingly, even sites exhibit-ing similar trophic positioning were characterized by substantialdifferences in  13 C distributions. Photosynthetic fractionation islikely to contribute to different  13 C signatures in different plantandalgalcommunities(SmithandEpstein1971;Smithetal.1976), and as is such, the make-up of primary producer communities islikely to influence the   13 C composition of the associated food web (Teeri and Schoeller 1979). Consistent with this relationship, the paired Weaver River and Pond sites showed no difference in  13 C distributions, despite significant differences in   15 N andtrophic position.  Table 1.   15 N and  13 C values from Painted Turtles ( Chrysemys picta ) and duckweed (  Lemna  sp.), as well as sample sizes,at each study location. n   15 N (‰)   13 C (‰)Study site  Lemna  sp.  C. picta Trophic positionof   C. picta Lemna  sp.  C. picta Lemna  sp.  C. picta Pristine Lake 3 5 2.36±0.13 0.50±1.93 5.14±0.45 −29.94±0.55 −25.52±0.41Northfield Pond 6 21 2.18±0.03 1.98±1.97 6.95±0.10 −25.20±0.57 −20.49±0.57 Weaver Pond 6 24 2.41±0.11 1.64±1.35 5.98±0.36 −25.49±0.52 −23.39±0.22 Weaver River 3 9 2.00±0.12 8.24±0.64 11.65±0.41 −23.71±0.48 −23.47±0.72Dakota River 3 10 1.88±0.09 8.62±0.14 11.60±0.30 −26.48±0.40 −20.42±0.30 Note:  Values are reported as means ± 1 SE.Hofmeister et al. 901Published by NRC Research Press    C  a  n .   J .   Z  o  o   l .   D  o  w  n   l  o  a   d  e   d   f  r  o  m  w  w  w .  n  r  c  r  e  s  e  a  r  c   h  p  r  e  s  s .  c  o  m   b  y   S   T   A   T   E   U   N   I   V   E   R   S   I   T   Y   N   Y  -   B   I   N   G   H   A   M   T   O   N  o  n   1   2   /   1   1   /   1   3   F  o  r  p  e  r  s  o  n  a   l  u  s  e  o  n   l  y .  The range of   C. picta  15 N and  13 C closely mirrored the rangesrecently reported for two freshwater emydid generalists, Com-mon Slider ( Trachemys scripta  (Schoepff, 1792)) and American Red- belliedTurtle(  Pseudemys rubriventris (LeConte,1830))(Pearsonetal.2013). While  Lemna  13 C values in our study were similar to thosefor  Lemna  sp. in other freshwater systems (Beaudoin et al. 2001; Zambrano et al. 2010), mean  Lemna   15 N in our study was lowerthan published   15 N values in the same systems. Differences in  Lemna  15 N between ours and other studies may reflect differentisotopic compositions of nitrogen sources.Turtles from the five sites showed identical sequences across thecontrol region marker, indicating a recent divergence time for theturtles in this study. In light of the mutation rate previously identi-fied for this marker in emydid turtles (1 mutation/170000 years;Freedberg and Myers 2012), these results suggest a very recentdivergence for the turtles at all five sites sampled. The lack of mutational divergence at a site that is characterized by a highmutation rate (Lahanas et al. 1994) suggests it is unlikely that genetic differences in metabolism could contribute to the differ-ences in  15 N values among turtles at different sites.Human activity has accelerated the nitrogen cycle and doublednitrogen input to the biosphere in the last century  ( Vitousek et al.1997; Gruber and Galloway 2008; Schlesinger 2009). For instance, agricultural watersheds are strongly impacted by anthropogenic Fig. 1.  There was a strong positive correlation between  15 N values (mean ± 1 SE) from Painted Turtles ( Chrysemys picta ) and duckweed(  Lemna  sp.) across collecting sites (  R  2 = 0.991,  p  = 0.0004).  Chrysemys picta  15 N varied significantly between all site comparisons except WeaverPond – Pristine Lake. Fig. 2.  Box plots of trophic position estimates of Painted Turtles ( Chrysemys picta ) in each study site. Trophic position of Dakota River turtles was significantly lower than all sites except Weaver River. Trophic position of Weaver River turtles was significantly lower than Weaver Pondturtles only. 902 Can. J. Zool. Vol. 91, 2013Published by NRC Research Press    C  a  n .   J .   Z  o  o   l .   D  o  w  n   l  o  a   d  e   d   f  r  o  m  w  w  w .  n  r  c  r  e  s  e  a  r  c   h  p  r  e  s  s .  c  o  m   b  y   S   T   A   T   E   U   N   I   V   E   R   S   I   T   Y   N   Y  -   B   I   N   G   H   A   M   T   O   N  o  n   1   2   /   1   1   /   1   3   F  o  r  p  e  r  s  o  n  a   l  u  s  e  o  n   l  y .
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