Oecologia (2002) 133:458–465 DOI 10.1007/s00442-002-1058-6
ECOPHYSIOLOGY
Maarit Pahkala · Anssi Laurila · Juha Meril
Effects of ultraviolet-B radiation on common frog Rana temporaria embryos from along a latitudinal gradient Received: 10 April 2002 / Accepted: 17 August 2002 / Published online: 2 October 2002 Springer-Verlag 2002
Abstract Interspecific variation in ultraviolet-B (UV-B) radiation tolerance in amphibians is well established, but little is known about the possible intraspecific variation in UV-B radiation tolerance within any species. We studied the effects of UV-B radiation on common frog Rana temporaria embryos originating from eight populations spanning a 1,200 km latitudinal gradient across Sweden. Newly fertilised eggs were exposed to three different UVB treatments [absent (no UV-B), normal (1.254 kJ m–2) and enhanced (1.584 kJ m–2, 26% above normal) levels] in a laboratory, and effects on survival, frequency of developmental anomalies, developmental rate and hatchling size were documented. UV-B radiation treatments did not have main factor effects on embryonic mortality or frequency of developmental anomalies. Survival to hatching was lower at higher latitudes, but it was independent of UV-B treatments. High UV-B treatment prolonged development time in five populations, whereas in one population development time was longest in the absence of UV-B. Even though the northernmost populations had the shortest development times, the interaction between latitude and development time was not significant. There was a significant populationUV-B interaction in hatchling size, indicating that hatchling size was negatively affected by the UV-B treatments in some of the populations. Hatchling size increased until midlatitudes and was again somewhat smaller at the northernmost latitudes, but this was independent of UV-B treatments. These results suggest that although R. tempoM. Pahkala ()) · A. Laurila · J. Meril Department of Population Biology, Evolutionary Biology Centre, Uppsala University, Norbyvgen 18d, SE-752 36, Sweden Present address: J. Meril, Ecological Genetics Research Unit, Department of Ecology and Systematics, P.O. Box 65, FIN-00014 University of Helsinki, Finland Present address: M. Pahkala, Department of Biology, University of Oulu, P.O. Box 3000, FIN-90014 Oulu, Finland, e-mail:
[email protected], Tel.: +358-8-5531218, Fax: +358-8-5531061
raria embryos are rather tolerant of UV-B radiation, and there is no clear latitudinal pattern to UV-B tolerance in this species, the sublethal effects of UV-B on embryonic development may differ among different populations. Keywords Amphibians · Embryonic development · Geographic variation · Sublethal effects · Ultraviolet-B
Introduction In recent years many amphibian populations have declined in various parts of the world (Wake 1991; Pechmann and Wilbur 1994; Blaustein and Wake 1995; Alford and Richards 1999). Several anthropogenic factors have been suggested to contribute to these declines, including habitat destruction, climate changes, chemical pollutants, introduced exotic species and increased levels of ultraviolet-B (UV-B) radiation (Alford and Richards 1999). However, the cause for the declines has been difficult to establish because often only some species are declining, whereas other species show no sign of decline (e.g. Blaustein et al. 1998; Alford and Richards 1999). For example, the increased UV-B (280–315 nm) radiation due to the depletion of the stratospheric ozone layer is a potential agent for the declines. UV-B radiation increases embryonic and larval mortality in some amphibian species [Grant and Licht 1995; Hays et al. 1996; Nagl and Hofer 1997; Ovaska et al. 1997; Ankley et al. 1998, 2000; Crump et al. 1999; Belden et al. 2000; Broomhall et al. 2000; Hkkinen et al. 2001; Kiesecker et al. 2001; see Blaustein et al. (1998) for a review], while some other species, like the common frog (Rana temporaria), appear tolerant to even high levels of UV-B radiation (Cummins et al. 1999; Langhelle et al. 1999; Meril et al. 2000a; Pahkala et al. 2000; Hofer and Mokri 2001; Hkkinen et al. 2001; but see Pahkala et al. 2001). Identifying the cause for amphibian declines may also become complicated if there are differential responses among populations of a single species (Blaustein et al. 1994; Corn 1998; Belden et al. 2000; Broomhall et al.
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2000; Pahkala et al., 2002). However, UV-B radiation is not a homogeneous stressor as its amount in the environment varies temporally and spatially (e.g. Madronich et al. 1995, 1998; Schindler et al. 1996; Meril et al. 2000b), and therefore, it could be expected that since different amphibian populations are exposed to different levels of UV-B radiation they can also differ in their tolerance to UV-B radiation. For example, due to both a naturally thicker ozone layer and decreasing solar inclination towards higher latitudes, mean yearly doses of UVB radiation for a given elevation, are lower at higher than at lower latitudes. Consequently, it has been generally assumed that organisms inhabiting higher latitudes can be expected to be more vulnerable to high levels of UV-B radiation if no adaptation to the local UV-B regime has occurred (Caldwell et al. 1980; Barnes et al. 1987; Gehrke 1998). This view was recently challenged by Meril et al. (2000b) who demonstrated that, due to differences in phenology, populations occurring at high latitudes might actually be exposed to much higher doses of UV-B radiation than those occurring at lower latitudes. For instance, in Scandinavian R. temporaria populations, the amount of UV-B radiation during the breeding season increases with increasing latitude, and the doses experienced by the northernmost populations are over 2 times higher than those in the south (Meril et al. 2000b). Therefore, if adaptation to a local UV-B regime has occurred, there appear to be good reasons to hypothesise that populations from higher latitudes may actually be more resistant to UV-B radiation than populations from lower latitudes. Several studies have compared UV-B radiation tolerance among different populations of the same species in field experiments (conducted in different localities, Blaustein et al. 1994, 1999; Kiesecker and Blaustein 1995; Corn 1998; Pahkala et al. 2000). While these studies are useful in comparing the UV-B radiation tolerance within the environments where the investigations were conducted (Blaustein et al. 1998), they may tell little about the possible intrinsic differences among the populations as the comparisons were not conducted under uniform environmental conditions. Only two studies have investigated population differences in UV-B tolerance under controlled laboratory conditions. Belden et al. (2000) found that larvae of the long-toed salamander (Ambystoma macrodactylum) from two different populations differed in their sensitivity to UV-B. Pahkala et al. (2002) found that R. temporaria embryos from two geographically widely separated populations differed in their response to UV-B in combination with low pH. Hence, there is clearly a need for additional studies focusing on geographic variation in UV-B radiation tolerance. UV-B radiation does not always induce direct mortality, and sublethal effects are probably common. UV-B is known to induce changes in behaviour (Belden et al. 2000; Blaustein et al. 2000) and increase the frequency of developmental anomalies (Grant and Licht 1995;
Kiesecker and Blaustein 1995; Blaustein et al. 1997; Langhelle et al. 1999; Pahkala et al. 2001). Also, several studies have found adverse effects on growth and development (Grant and Licht 1995; Belden et al. 2000; Smith et al. 2000; Meril et al. 2000a; Pahkala et al. 2000, 2001, 2002; Hkkinen et al. 2001). The aim of this study was to compare under controlled laboratory conditions the embryonic UV-B tolerance among eight common frog populations situated along a latitudinal gradient within Sweden. As the amount of UVB radiation during the breeding season increases towards the north (Meril et al. 2000b), we predicted that the northern populations should be more tolerant to UV-B than southern populations as the former experience higher UV-B doses in nature. We recorded survival, frequency of developmental anomalies and size and age at hatching. In addition, we investigated latitudinal variation in these variables.
Materials and methods The study species and populations The common frog is the most widespread anuran in Europe (Miaud et al. 1999). Typical breeding locations in Scandinavia vary from temporary pools to bogs and shore marshes of large lakes. The breeding season commences in late March to early April in southern Sweden, and in mid-June in northern Sweden. The eggs are laid in shallow water with the uppermost eggs typically reaching the water’s surface. Depending on the water temperature the eggs usually hatch within 2 weeks. Adult R. temporaria were captured at eight different localities along a 1,200-km transect from southern to northern Sweden in spring 1999 (Table 1; Fig. 1). Commencement of the breeding season between the southern and the northernmost localities differs by approximately 60 days (J. Meril, personal observation), and at the start of the respective breeding seasons there is about twice as much UV-B radiation in the north as compared to the southernmost location (Meril et al. 2000b; Table 1). Mean ambient temperature during the 2-week period following the onset of egg laying in these localities varies from 4.9 to 9.5C (Table 1). In all the localities, two to eight pairs of adult frogs (see Table 1) were collected from spawning sites at the onset of the respective breeding seasons and transported to the laboratory in Uppsala. Experimental design Eggs used in the experiments were obtained by using artificial fertilisation following the procedure of Berger et al. (1994). Each male was artificially mated with one female resulting in two to eight full-sib families (clutches) per population (Table 1). Artificial mating provided homogeneous material (eggs experienced the same treatment before the experiment and entered the experiment at the same developmental stage) for population comparisons and ensured that the eggs had no priori exposure to UV-B radiation. Any damaged and/or unfertilised eggs were not used in the experiments. After fertilisation, the eggs (
