Acta Herpetologica 10(2): 85-91, 2015 ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah DOI: 10.13128/Acta_Herpetol-16297 Variation of growth rate and survival in embryos and larvae of Rana temporaria populations from the Pyrenees Neus Oromi1,2,*, Sebastià Camarasa1, Isabel Sanuy1, Delfi Sanuy1 1 Escola Tècnica Superior d’Enginyeria Agrària, Departament de Producció Animal (Fauna Silvestre), University of Lleida, Av. Rovira Roure 191, 25198 Lleida, Spain. *Corresponding author. E-mail: noromi@ulg.ac.be 2 Laboratory of Fish and Amphibian Ethology, Behavioural Biology Unit, Department of Biology, Ecology and Evolution, University of Liege, 22 Quai van Beneden, 4020 Liege, Belgium Submitted on 2015, 4th June; revised on 2015, 2nd October 2015; accepted on 2015, 5th October Editor: Sebastiano Salvidio Abstract. Variations on embryonic and larval life history traits of ectotherm organisms are strongly affected by tem- perature conditions. However, these effects can vary between species and populations depending on the mechanisms that act in a determinate local habitat. In the present study, we analysed the effects of temperature on several embry- onic and larval traits (survival, development and growth rate until the metamorphosis) of Rana temporaria in two populations living at different altitude (1540 and 2100 m) in the Pyrenees. Five spawns from each population were distributed in a common garden experiment at different temperature treatments according to the normal tempera- ture range that tadpoles might experience in the field and also considering a high treatment (24 °C) to test a possible effect of global warming. Like in other studies of the same species in a latitudinal gradient, the temperature effects depended on the analysed trait. Our results support the general rule that the rate of development is faster at higher temperatures, although survival was significantly affected by the highest temperature in the highland population. Size varied at embryonic and larval stages and was largest at metamorphosis in the highland population. In concordance, the growth rate was higher in the highland population suggesting a countergradient variation in response to the short growing season. However, this possible adaptation can be altered in a global warming scenario with an increase of mortality and limited growth. Keywords. Rana temporaria, development, growth, altitudinal variation. INTRODUCTION Variation in climatic conditions determines intraspe- cific differences in life histories especially in ectotherm organisms. In general, low temperature reduces their physiological rates, decreasing the development and growth rates at higher latitudes and altitudes. However, many studies have found increased growth and develop- ment rates at higher latitudes and altitudes (e.g. Conover and Schultz, 1995; Arendt, 1997). The effects of tempera- ture in anuran tadpoles can influence some traits that are basic to population survival in one specific habitat. In addition, the warmer waters can compromise sur- vival because of decreased oxygen availability, oxidative stress due to higher metabolic rate and the build-up of microbes from decomposing food or nitrogenous waste products (e.g., Courtney Jones et al., 2015). The increased temperature can reduce the metamorphic size in some species (e.g., Álvarez and Nicieza, 2002: Discoglossus gal- ganoi; Orizaola and Laurila, 2009: Rana lessonae) whereas in other species growth is accelerated by high tempera- tures (e.g., Arendt and Hoang, 2005: Spea hammondi; Sanuy et al., 2008: Bufo calamita). The mechanisms that determine the variation of these larval life history traits can be understood in a local habitat scale. Therefore, intraspecific studies of geographic variation have pro- 86 Neus Oromi et alii vided evidences of the occurrence of microevolution as a response to local ecological conditions (e.g., Conover and Schultz, 1995; Huey et al., 2000; Laugen et al., 2005). Several evolutionary models can explain the occur- rence of the different mechanisms that determine the variation of larval life history across a latitudinal or alti- tudinal gradient (Yamahira and Conover, 2002). Environ- mental influences and microevolutionary pressures can act synergistically on the phenotypic variation of life his- tory traits (cogradient selection) when both factors tend to either reduce or enhance the trait in question occur- rence of microevolution as a response to local ecological conditions (e.g., Conover and Schultz, 1995). Considering this hypothesis, organisms are adapted to the tempera- ture that they most commonly experience in the natural environment (Levinton and Monahan, 1983; Lonsdale and Levinton, 1985). Therefore, in an altitudinal gradient, populations living at low altitudes are expected to grow faster at high temperatures, whereas high altitude popu- lations can show a higher growth rate at a low tempera- ture. However, if the phenotypic response does not reflect the microevolutionary process responsible for the popu- lation genetic differentiation (Arendt and Wilson, 1999; Ghalambor et al., 2007; Crispo, 2008), the environmental factor can be antagonistic against the effect imposed on the phenotypic variation by natural selection (Conover and Schultz, 1995). From this perspective, considering the breeding period along an altitudinal gradient, as the length of the growth season declines across higher alti- tudes, the tadpoles living at high altitudes have less time to grow and develop than those in low altitudes (Cono- ver and Schultz, 1995). Consequently, highland popula- tions are expected to have a higher capacity for growth and development in all temperatures, in order to be able to compensate for the shorter growth season. The essen- tial prediction of this hypothesis is that there should be an inverse relationship between the length of the growth season and the capacity for growth and development (Conover and Schultz, 1995; Yamahira and Conover, 2002). This phenomenon is known as “countergradient variation” (Conover and Schultz, 1995; Levins, 1969). Although larval growth and development rates have been considered important in the determination of per- formance during later life stages (Mousseau and Fox, 1998; Lindström, 1999), very little is known about life his- tory variation in embryonic and larval traits along altitu- dinal gradients. In Rana temporaria, Muir et al. (2014a) in Scotland reported a phenotypic plasticity variation in an altitudinal gradient. In our study we also analysed a phe- notypic variation depending on temperature treatments, in the case of high temperatures than those recorded in the field. Global average surface temperature is predicted to further rise by 2 to 6 °C at the end of the 21st century (IPCC, 2007). Global warming can significantly change the behaviour, growth rate, and reproductive phenology of a species, specially affecting the ectotherms organisms (Brattstrom, 1963). There is a notable lack of knowledge about the impact of global warming on the survival and life history traits of the populations from cold habitats. As high latitude ectotherms can be highly vulnerable to cli- mate warming in temperate zones (Gerick et al., 2014) we expect a similar effect at high altitudes. In this study we want to investigate the effects of temperature in a large-wide distributed European species, the common frog Rana temporaria, across an altitudinal gradient in the Pyrenees. Previous studies on this anuran species have focused in embryonic and larval life history traits at latitudinal scales. Several works have found that larval growth and development rates increase with lati- tude (Merilä et al., 2000; Stählberg et al., 2001; Laugen et al., 2002; Laurila et al., 2001, 2002). However, other studies show that the variation in the embryonic develop- ment and growth in R. temporaria cannot be explained in terms of a latitudinal gradient in season length whereas adaptation to a latitudinal variation in temperature might contribute to explain the variations observed (Laugen et al., 2003b). Lindgren and Laurila (2005, 2010) found increased growth rate at higher latitudes, evidencing that the populations from higher latitudes had higher growth efficiency. In our study, we analyse the effects of tempera- ture on embryonic and larval life history traits of R. tem- poraria across an altitudinal gradient in the Pyrenees. The length of breeding season declines, as well as the ambi- ent temperature, from the low to the highland popula- tions. We analyse if seasonal time constraints are mainly responsible for the observed variations or if the adapta- tion to the prevailing temperature is the important factor. In addition, we aim to assess the survival effect at high temperatures in larvae of R. temporaria. At high altitude, the tadpoles of R. temporaria appear to have the poten- tial to adapt physically to surviving at low temperatures (Muir et al., 2014a) but what occurs when the tempera- ture exceeds their normal exposure range is unknown. MATERIAL AND METHODS Study zone The study zone was situated in a pasture area of the Vall d’Aneu (42°37’N, 1°03’E) in the Catalonian Pyrenees (Ibe- rian Peninsula). The lowland population was located near a stream (Riera del Tinter) at 1540 m. The highland population was situated in the same valley in a breeding site near a small river (Les Cabanyes) at 2100 m. Both populations reproduce 87Growth rate and survival in larvae of Rana temporaria in temporary ponds formed as a consequence of the thawing of snow and ice in spring. The climate is typical of temperate mountain regions, with short bursts of heavy rainfall in April and May, and stable periods of high pressure between Septem- ber and November. The temperature conditions of the zone have been extrapolated from the data of the National Park of Aigüestortes in the Pyrenees (from 2005 to 2008) at altitudes of 1600 and 2000 m. The temperatures during spring and summer varied from 3.8 to 22 °C at 1600 m and 1.1 to 19.5 °C at 2100 m (from May to September; minimum and maximum air temperature respectively). We considered the length of the growth season as continuous period, from spring (May) to winter (October) where mean air temperature exceeds +5 °C. It was approx. of 120 days for the lowland population and 90 days for the highland population. We considered that breed- ing did not occur below 5 °C, as reported Muier et al. (2014) on populations of R. temporaria at high altitude in Scotland. The onset of the breeding season differs between populations (the highland population reproduced 1 month after the low- land population). Experimental design Rana temporaria eggs were collected on April 5th and May 5th 2012, from the lowland and highland population respec- tively, at embryonic stage 0-3 of Gosner (1960). The eggs were taken to the laboratory of the University of Lleida (Spain) and immediately used in the experiment. The temperature treat- ments (16, 20 and 24 °C) were selected according to the normal temperature range that tadpoles might experience in the field and also considering a high treatment (24 °C) to test a pos- sible effect of global warming in the growth and development of R. temporaria in the Pyrenees. The experiment was formed by 3 controlled temperature systems: 16, 20 and 24 °C. Each temperature system was formed by 4 plastic boxes (57 × 77 × 20 cm) of 40 litres connected between them to avoid tempera- ture fluctuation. Eggs from each population (represented by 5 spawns per population) were randomly distributed in the dif- ferent plastic boxes and individualised (225 larvae per popula- tion) in floating plastic glasses (0.5 L) in each temperature con- dition. The remained eggs were released in the same site where were collected. The temperature in each plastic box (12 plastic boxes, 4 per temperature) was measured every day (SD = ± 0.3 °C). Water of each plastic glasses was changed every three days. When tadpoles arrived at stage 25, they were fed with fish food ad libitum and excess food was removed every day. Larval mor- tality was monitored every day. The body length (without the tail (length) of each larva in the different treatments was also regularly measured, using a digital camera and a millimetre scale. We obtained the measures of length with the Corel Draw 7.0 program using the “dimensioning lines” tool to measure the distance between two points. The distance was corrected using the millimetre scale available in each digital photo. The response variables measured from each tadpole were: 1) Age at hatching (defined as the number of days between Gosner stages 0-3 and 25), 2) Age at metamorphosis (defined as the number of days between Gosner stages 0-3 and 42), 3) size at hatching (measured by body length at stage 25), 4) size at metamorphosis (measured by body length at stage 42) and 5) larval growth rate (between Gosner stages 25 and 42 divided by the days between these two stages). At the end of the experiment, all the survival animals were released to the field. Statistical analyses The laboratory experiment was a factorial design with pop- ulation (lowland and highland) and temperature (16, 20 and 24 °C) as factors. All the data of the response variables were first tested for normality and variance heterogeneity before analyses. Age at hatching and metamorphosis, and growth rate were log- transformed to archive normality. Survival was performed on arcsin-transformed proportions, which effectively normalized the error variances. The effects of temperature and population, as well as their interaction, on survival and size at hatching and metamorphosis were analysed in a 2-factorial ANOVA. To test the differences in the egg size between populations in the begin- ning of the experiment, we used a 1-factorial ANOVA analysis. All the analyses were based on the procedures of the statistical package JMP 9.0.1 with a significance level of alpha = 0.05. RESULTS Survival The survival at hatching was affected by population and temperature treatment without significant interaction (lowland population: 99, 98.9 and 96% at 16, 20 and 24 °C; highland population 95.6, 95.4 and 82% respectively; Table 1). At the end of the study, the survival at meta- morphosis was lower in the highland population (92, 93.3 and 84% at 16, 20 and 24 °C respectively) than in the lowland population (98.6, 98.6 and 94.6%). Although, the highest temperature reduced the survival in both popula- tions, there were not statistical differences between tem- perature treatments (Table 1). Development time Age at hatching and metamorphosis varied signifi- cantly between temperature treatments without popula- tion effects at early time of development (Table 1, Fig.1A, B). The populations had higher age at hatching and meta- morphosis as temperature treatment increased. The sig- nificant interaction between temperature and population factors at age at metamorphosis shows that temperature treatment did not affect in the same level the two popula- tions. In fact, in contrast to the results in the other tem- peratures, the highland population developed slower than the lowland population at 24 °C. 88 Neus Oromi et alii Size and growth rate At the beginning of the experiment, the eggs of the highland population, 2.48 ± 0.39 (SD) mm, had similar size than those in the lowland population, 2.39 ± 0.11 (SD) mm (1-factorial ANOVA; F = 2.76, P = 0.09). The population effect was significant on size at hatching and metamorphosis. The temperature was significant on size at metamorphosis but not at hatching (Table 1, Fig. 2A,B). Size at hatching and metamorphosis varied depending on population origin and temperature treatment (Table 1, Fig. 2A,B). However, the growth rate, which allows to measure the exploitation of resources, was significantly higher in the highland population (2 factorial ANOVA, F1,188 = 101.66, P < 0.00001) without temperature treat- ment effects (F2,188 = 1.41, P = 0.247) and interaction (“temperature*population”: F2,188 = 2.93, p = 0.056, Fig. 3). DISCUSSION The present work shows a relevant effect of the tem- perature on the development and growth of Rana tem- poraria that depends on the altitude. Mortality increased weakly at highest temperature in all populations, especial- ly notable at highest temperature in the highland popu- lation. This is probably due to the fact that the highland population is unlikely exposed in the nature to tempera- tures above 22 °C. As it was found in other amphibian species (Gerick et al., 2014) in a global warming scenario, Table 1. Results of ANOVA for the effects of temperature (16, 20 and 24 °C) and population (lowland and highland) on survival, age and size at hatching and metamorphosis of Rana temporaria tadpoles. (SS= Sum of Squares; df= degrees of freedom). Response Source SS df F P Survival at hatching Population Temperature Temperature x Population 7414.27 2276.57 1073.53 1, 835 2, 835 2, 835 30.54 4.68 2.21 < 0.001 0.009 0.110 Age at hatching Population Temperature Temperature x Population 0.02289 1.41241 0.02936 1,1499 2,1499 2,1499 1.81 57.57 1.20 0.174 < 0.0001 0.305 Hatching size Population Temperature Temperature x Population 415.789 24.7488 49.0953 1, 330 2, 330 2, 330 68.04 1.88 3.72 < 0.0001 0.154 0.025 Survival at metamorphosis Population Temperature Temperature x Population 362.049 244.136 244.136 1, 690 2, 690 2, 690 3.99 1.35 1.35 0.045 0.260 0.260 Age at metamorphosis Population Temperature Temperature x Population 5.89946 13.5599 1.43157 1, 694 2, 694 2, 694 28.14 32.34 3.41 < 0.0001 < 0.0001 0.033 Metamorphosis size Population Temperature Temperature x Population 42.4891 10.4598 42.4891 1, 188 2, 188 2, 188 5.02 0.62 2.50 0.026 0.541 0.085 Fig. 1. Mean days (± SD) of development time of two Rana tempo- raria populations at three temperature treatments. A) Age at hatch- ing and B) age at metamorphosis. 89Growth rate and survival in larvae of Rana temporaria some populations will experience maximum summer tem- peratures above their maximum thermal limit that can promote the disappearance of these populations. However, others studies about temperature tolerance (Duarte et al., 2012) at different stages and altitudes are needed to evalu- ate the possible effects of global warming in the perpetua- tion of R. temporaria in its present distribution. We found different temperature effects and variations that depend on the analysed trait, as e.g., Lindgren and Laurila (2005) showed in a latitudinal gradient in Scandi- navian R. temporaria populations. For example, while age at metamorphosis increased at low temperatures and in the highland population, size was similar between tem- perature treatments at hatching and higher in the low- land population. In contrast, the size at metamorphosis was not affected by the temperature, being larger in the highland population. The temperature affected the earli- est stages of development but the population effects or altitudinal effect, began to be notable after embryonic stages, past the stage 25. It is possible that the time con- straint imposed on embryonic stages is not as severe as in the larval development, because the larvae may com- pensate the delays in hatching (Räsänen et al., 2002). In addition, a high development rate can limit the hatch- ling size, that is a more important fitness factor than age at hatching (Laugen et al., 2003a). A larger hatching size is often beneficial because it increases competitive abil- ity and in many systems brings a survival advantage or other improvements in later fitness (Kaplan, 1998; Pech- enik et al., 1998; Lindström, 1999). In our study, the dif- ferences on age at hatching between populations are not much notable and the highest hatching size in the low- land population seems to be an altitudinal effect. Others studies on R. temporaria have shown that embryos from low altitude develop slower than those from higher alti- tudes (Angelier and Angelier, 1968; Martin and Miaud, 1999). However, Pahkala et al. (2002) and Laugen et al. (2003a) did not find a clear pattern of embryonic devel- opment across a latitudinal cline (Scandinavia). In our study, we found clearly that development rates increase with altitude only at low temperature (16 °C), similarly to the results showed with latitude in R. temporaria of Scandinavia (Martin and Miaud, 1999; Merilä et al., 2000; Laurila et al., 2001, 2002) and in an altitudinal range in Scotland (Muir et al., 2014a). The growth rate showed a clear variation, suggest- ing an increase of this trait along the altitudinal gradient across the Pyrenees. Other authors found similar results in the same species across a latitudinal gradient in Scan- dinavia, but in those cases, the development rates of R. temporaria increased in the northern populations (e.g., Merilä et al., 2000; Laugen et al., 2003b; Lindgren and Laurila, 2005). Tadpoles in the highland populations can exhibit higher activity of the enzymatic levels deriving in a larger size (latitudinal gradient: Laurila et al., 2008; altitudinal gradient: Muir et al., 2014a) that increases the competitive ability of high altitude tadpoles as com- pared to low altitude conspecifics. In addition, the higher Fig. 2. Average size (± SD) at different temperature treatments of two populations of Rana temporaria. A) Hatching size and B) meta- morphosis size. Fig. 3. Growth rate (GR) (± SD) of two populations of Rana tempo- raria at different temperatures. 90 Neus Oromi et alii growth rate was maintained in all temperature treat- ments, suggesting an adaptation to season length rather than to prevailing temperature (Conover and Schultz, 1995; Laugen et al., 2003b; Palo et al., 2003). Survival at high altitude is probably facilitated by mechanisms that permit faster growth rate in R. temporaria (Muir et al., 2014b). Overall, in the line of a large number of ectotherms studies, our results support the general rule that devel- opment rate is faster at higher temperatures. However, hatching size is not affected by temperature treatments, which is the opposite to the pattern commonly found in ectotherms (Atkinson and Sibly, 1997). Probably the energetic costs of development at low temperature lim- it a larger size that can be derivate of a long embryonic development. As Muir et al. (2014b) reported in the alti- tudinal gradient of Scotland, we found a higher larval growth rate in the highland population that suggests an adaptation that has occurred to maximize growth during the short growing season. However, this possible adapta- tion can be altered in a global warming scenario with an increase of mortality and limited growth. ACKNOWLEDGMENTS Thanks to Pepe Guillen for the field work and to Lluis Camarero for providing the meteorological data. 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