Present address: College of Life Science, Guangxi Normal University, Guilin, 541004, Guangxi, China
Insular shifts in body size of rice frogs in the Zhoushan Archipelago, China
Article first published online: 27 JUN 2006
Journal of Animal Ecology
Volume 75, Issue 5, pages 1071–1080, September 2006
How to Cite
WU, Z., LI, Y. and MURRAY, B. R. (2006), Insular shifts in body size of rice frogs in the Zhoushan Archipelago, China. Journal of Animal Ecology, 75: 1071–1080. doi: 10.1111/j.1365-2656.2006.01126.x
- Issue published online: 27 JUN 2006
- Article first published online: 27 JUN 2006
- body size;
- insular shift;
- resource availability;
- prey size;
- 1Differences in body size between mainland and island populations have been reported for reptiles, birds and mammals. Despite widespread recognition of insular shifts in body size in these taxa, there have been no reports of such body size shifts in amphibians.
- 2We provide the first evidence of an insular shift in body size for an amphibian species, the rice frog Rana limnocharis. We found significant increases in body size of rice frogs on most sampled islands in the Zhoushan archipelago when compared with neighbouring mainland China.
- 3Large body size in rice frogs on islands was significantly related to increased population density, in both breeding and non-breeding seasons. Increases in rice frog density were significantly related to higher resource availability on islands. Increased resource availability on islands has led to higher carrying capacities, which has subsequently facilitated higher densities and individual growth rates, resulting in larger body size in rice frogs. We also suggest that large body size has evolved on islands, as larger individuals are competitively superior under conditions of harsh intraspecific competition at high densities.
- 4Increases in body size in rice frogs were not related to several factors that have been implicated previously in insular shifts in body size in other taxa. We found no significant relationships between body size of rice frogs and prey size, number of larger or smaller frog species, island area or distance of islands from the mainland.
- 5Our findings contribute to the formation of a broad, repeatable ecological generality for insular shifts in body size across a range of terrestrial vertebrate taxa, and provide support for recent theoretical work concerning the importance of resource availability for insular shifts in body size.
Island populations of terrestrial vertebrates often show increases or decreases in body size compared with mainland relatives (Foster 1964; Schoener 1969; Lomolino 1985; Schwaner & Sarre 1988; Case & Schwaner 1993; Alder & Levins 1994; Clegg & Owens 2002). Several factors have been implicated in generating insular shifts in body size, including resource availability, competition and predation (Grant 1968; Schoener 1970; Case 1978; Heaney 1978; Lawlor 1982; Melton 1982; Case & Schwaner 1993; Dayan & Simberloff 1994; Whittaker 1998; Robinson-Wolrath & Owens 2003). Despite widespread recognition of insular shifts in body size in reptiles, birds and mammals, there have been no reports of such body size shifts in amphibians. In the present study, we show for the first time insular increases in body size in island populations of an amphibian, the rice frog Rana limnocharis, found in the Zhoushan archipelago in the East China Sea. Further, we explore the relative importance of several key ecological factors for body size increases in rice frogs on islands.
Recent theoretical work has predicted a network of ecological associations leading to shifts in adult body size on islands (Palkovacs 2003). The work is based on life-history theory (Stearns 1992), and considers that food availability and predation are two important factors influencing a species’ life-history characters. Low resource availability can slow growth rates, delay age at maturity and even result in reduced body size at maturity (Wilbur 1980; Baker 1982; Anholt 1991). Reduced predation may increase foraging rates, resulting in an increase in age and body size at maturity (Stearns 1992; Ball & Baker 1996). In contrast, high resource availability and increased predation pressure can produce shifts in these life-history characters, especially body size, in the opposite direction. Under conditions where resource limitation predominates over extrinsic mortality, an increase in resource availability − which leads to a higher carrying capacity − is predicted to lead to an increase in body size through increases in population density and individual growth rates (Alder & Levins 1994; Palkovacs 2003).
Increased population density also favours the evolution of large body size, given that intraspecific competition becomes more intense at high population densities, and that large body size provides a competitive advantage under these conditions (Case 1978; Melton 1982). Changes in resource availability may result in phenotypically plastic responses in body size, as well as genetic responses (Palkovacs 2003). Thus, the effects of resource availability on plastic responses in body size can be assessed on the basis of a single generation.
Insular shifts in vertebrate body size might also be related to changes in prey size (Van Valen 1965; Grant 1968; Schoener 1969; Roughgarden 1972; Lister 1976; Heaney 1978; Dayan & Simberloff 1994; Petren, Grant & Grant 1999; Meiri, Dayan & Simberloff 2004). The hypothesis is that the availability of small- and large-sized prey on islands should change in relation to the absence of small or large competitors. Several studies have examined this idea by relating vertebrate body size to prey size and the number of competitors missing from islands. However, studies exploring this idea have usually been performed without statistical analyses and have found equivocal support for the hypothesis (Schoener 1969; Malmquist 1985; Schwaner & Sarre 1988, 1990; Schwaner 1990; Case & Schwaner 1993; Dayan & Simberloff 1998).
Adler & Levins (1994) constructed a conceptual model that predicted insular population density and body size increasing with increasing island isolation, and decreasing with increasing island area. The model assumes that the effects of isolation are direct by limiting dispersal and numbers of predators and competitors. In addition, habitat structure is predicted to increase in diversity with increasing island area. Research on carnivores has provided no support for a consistent relationship between island area or isolation and body size (Meiri, Dayan & Simberloff 2005; Meiri, Simberloff & Dayan 2005). Other authors have addressed interactions among competition, changes in seasonal resource allocation and feeding niche width to explain dwarfism of elephants on islands (Raia, Barbera & Conte 2003).
Here, we test the importance of resource availability in generating the observed insular increase in body size in the rice frog. If resource availability is important for increased body size according to the life-history model (Palkovacs 2003), we should observe that increases in resource availability are related to insular increases in population density of the rice frog, and that increases in population density of rice frogs are related to increases in body size of rice frogs on islands. We also test whether insular increases in prey size and insular differences in the number of competing frog species present on islands are related to insular variation in body size in rice frogs. In addition, we test whether island area and the distance of islands from the mainland are related to body size in rice frogs. Because resource (prey) availability and prey size often exhibit seasonal variation, we perform our tests of these predictions during both breeding and non-breeding seasons of the rice frog.
Materials and methods
The rice frog is an ideal candidate with which to test predictions for several reasons. First, Zhoushan archipelago belongs to land-bridge islands, and rice frog populations on the islands were part of the mainland population as late as the late Pleistocene (Wang & Wang 1980; but see below). Because seawater is harmful to amphibians (Gadow 1901), frogs cannot disperse among islands and the mainland (Yiming, Niemelä & Dianmo 1998). Morphological variation of frog populations among islands has evolved independently, and is strongly determined by the local environments of each island. Secondly, the rice frog is one of the most abundant amphibians in the study area (Huang 1990). Large sample sizes of frogs can be collected with which to address body size shifts in different seasons. This eliminates the potentially confounding influence of small sample size on estimates of insular shifts in body size (Case & Schwaner 1993). Thirdly, distributions of frog species in the study area are well documented (Gu & Jin 1985; Huang 1990; Yiming et al. 1998). Finally, the diet of the rice frog is composed mainly of arthropods (Zhang et al. 1966). Arthropod availability and size can change dramatically with seasons and can be quantified conveniently (Wolda 1988).
Post-metamorphic rice frogs are largely terrestrial and found commonly in grass, crops and stones around rice fields, ponds, bogs and ditches (Huang 1990). On the mainland and archipelago, frogs emerge from hibernation at the end of March to early April. Breeding occurs between the end of April and the end of August. Females lay eggs in rice field, bogs, ditches and temporary waters, but not in deep ponds or flow streams. They characteristically lay multiple clutches of eggs. Tadpoles in water take about 1 month to complete metamorphosis. Hibernation usually begins in early November (Huang 1990). Once rice frogs reach adulthood they can continue to grow, but growth rates in adults are lower than in juveniles (Deng 1990).
The rice frog is not hunted in the study area (Yiming, Zhengjun & Duncan 2006). In addition, species richness of predators of rice frogs, which include small carnivores, wading birds and snakes, is much lower in the Zhoushan archipelago than in equivalent areas of mainland (Huang 1990; Zhu 1990; Zuge 1990).
The Zhoushan archipelago (29°31′−31°04′ N and 121°30′−123°25′ E) is comprised of 1339 islands located in the East China Sea (Fig. 1). Islands in the archipelago separated from mainland China about 7000–9000 years ago in the late Pleistocene (Wang & Wang 1980). Topography, climate and vegetation of the archipelago are similar to the mainland (Zhou 1987; Yiming et al. 1998). The mainland and archipelago are covered with subtropical evergreen broad-leaved forest. Both the mainland and archipelago are in the subtropical monsoon zone (Ningbo City Government 1991; Zhoushan City Government 1992), and experience highly seasonal weather conditions. Spring is warm with high rain between late March and mid-June, while summers are hot and rainy during mid-June to late September. Autumn is typically dry, beginning in late September and ending in late November. Freshwater ponds, pools, rivers and reservoirs are numerous on the islands, and are of importance for amphibians as their breeding sites. Larger islands usually have more freshwater resources. No endemic vertebrate species are found on the islands.
collection of study materials
The study was conducted on the mainland and on seven island sites (Zhoushan, Daishan, Taohua, Mayi, Xiashi, Liuheng and Fodu) (Fig. 1). Zhoushan (468·7 km2) and Daishan (100 km2) are the two largest islands in the archipelago (Table 1). We collected data on body size and density of rice frogs at all study sites during breeding (mid-May to mid-June) and non-breeding (September) seasons. At the same time, data on prey availability and size and the size of prey in the diet of frogs were collected. Because adult frogs can continue to grow after maturity, time of sampling may have an effect on body size of individuals sampled. To reduce such an effect, we began by collecting field data on the mainland, then proceeded to collect data on the islands in a randomly determined order. After sampling of the islands was completed, we resampled on the mainland and used mean values of the two sampling periods for the mainland for all attributes measured.
|Zhoushan||Daishan||Liuheng||Taohua||Xiashi||Mayi||Fodu||Males SV (mm)||Females SVL (mm)|
|Distance to mainland (km)||9·0||37·0||7·0||8·8||13·2||11·5||7·0|
|Number of larger frog species||6||5||4||3||3||4||2|
|Number of smaller frog species||3||2||2||2||2||1||1|
|Bufo bufo gargarizans||+||+||+||+||+||+||69·0||96·7|
Data were also collected on island area, distance to the mainland of each island and frog species richness and identity for each island (Table 1). Distance to mainland was measured using a map of the region (scale 1 : 400 000). Island areas were obtained from Chen (1989). Information on species richness and identity of frog species was collected from published records (Gu & Jin 1985; Yiming et al. 1998). Species richness on the islands (ranging between n = 3 and 10 species for our study sites) is poorer than the neighbouring mainland (n = 14 species) (Huang 1990; Yiming et al. 1998). The four species missing from the islands include the large-bodied species Rana spinosa and R. tigrina, the mid-bodied species R. schmackeri and the small-bodied species Microhyla heymonsi.
We used the line transect method to survey rice frog densities (Jaeger 1994). Each transect was 2 m wide and 100–200 m long, and situated along accessible edges of rice fields and shorelines of ponds and ditches. Bullfrogs R. catesbeiana have invaded all study islands except Mayi (Yiming et al. 2006), where they have invaded only a part of the island. To avoid the potential effects of bullfrog predation on local frogs, our line transects were situated in areas far from bullfrog invasion. We set one line transect at each study site. Transects were searched at night (19:00–21:30 h) with a 12-V DC lamp, and each frog encountered was counted. Search speed was approximately 1–2 km h−1. Frogs were captured by hand, labelled with a toe-tag, placed in separate plastic bags with holes (for air flow) and returned to the laboratory for further analysis. A description was made of the habitat where each frog was captured. Captured frogs were released at their capture site the following morning. Males were identified based on secondary sexual characteristics (e.g. nuptial pads and black pigment on the throat). Due to independent evolution of rice frog body size on each island and the mainland, individuals with body mass less than the minimum body mass of male rice frogs at a location were considered juveniles at that location, and frogs lacking male characteristics were considered females. Density of rice frogs was calculated as the number of rice frogs per total length of line transect.
Calipers were used to measure snout–vent length (SVL) and head width (across the base of the head at its widest point) of captured frogs, and each frog was weighed to the nearest 0·1 g. Because body size is influenced by sex, we calculated body sizes of males and females separately. Stomach contents of adult frogs were flushed by stomach flushing (see Measey 1998). Flushed contents were captured in a plastic container and filtrated immediately with gauze, then preserved in 75% alcohol. Stomach contents were spread in a Petri dish and all prey items were identified to the lowest possible taxonomic level (usually Family) and life stage with the aid of a magnifier (8×) and references. The length and width of each prey item was measured with a caliper (to the nearest 0·02 mm).
After sampling frogs, we estimated abundance of prey availability with sweeping samples (McCoy 1990). Trapping lines were fixed along line transects where rice frogs were captured. We conducted 100 sweeps with a net along each trapping line at each study site. Animals in the sweep net were placed into plastic cups with ethyl acetate and returned to the laboratory for further analysis. All prey captured by sweeps were identified to the lowest possible taxonomic level (usually Family), counted and measured (length and width with a caliper to nearest 0·02 mm) individually. The volume of each food item was calculated using the formula for an ellipsoid (see Magnusson et al. 2003): food volume = 4/3π× (length/2) × (width/2)2. We used the total volume of prey as the measure of prey availability. Prey were included in our measurements only if their size was equal to or below the maximum size of prey found in our stomach content analysis of rice frogs. The largest prey of rice frogs were earthworms. The diet was composed of arthropods (76·29%, volume percentage), annelids (14·67%), molluscs (5·64%) and frogs (3·40%).
We used t-tests to examine differences in body size between the mainland and each island population. Differences in body size, density, food availability (available food volume) and available food size between breeding and non-breeding seasons were tested using t-tests for paired samples.
We defined coexisting frog species as larger (or smaller) competitors to the rice frog if both males and females of the species were larger (or smaller) than those of the rice frog on the mainland (Table 1). We used the number of larger species and of smaller species present on islands as indices of missing competitors relative to rice frog body size. A higher number of larger (or smaller) species present on an island may mean fewer larger (or smaller) species missing from the island. We implemented single variable regressions and stepwise multiple-variable regressions to determine relationships between body size (response variable) and rice frog density, prey availability, prey size, number of larger competitor species and of small competitor species, island area (ln-transformed) and distance to mainland. Two sets of regression analyses were performed: one that included both islands and mainland, and one that considered only islands. All statistical analyses were performed using the spss statistical package (SPSS Inc. 1997).
body size comparisons between mainland and islands
We found significant differences in body size between mainland and all island populations of rice frogs (Table 2). In both seasons, female frogs on six islands (Daishan, Liuheng, Taohua, Xiashi, Fodu, Mayi) were, on average, significantly larger than frogs on the mainland. In the breeding season, male frogs on five islands (Daishan, Liuheng, Taohua, Xiashi, Mayi) were significantly larger than frogs on the mainland. In contrast, both sexes were significantly smaller-bodied on Zhoushan compared with the mainland. In the non-breeding season, male frogs on five islands (Daishan, Taohua, Xiashi, Fodu, Mayi) were significantly larger than frogs on the mainland.
|Season and location||Females||Males|
|Mass (g)||Mass (g)|
|(mean ± SE) (n)||P (t-test)||Trend||(mean ± SE) (n)||P (t-test)||Trend|
|Mainland||7·00 ± 0·32 (95)||4·94 ± 0·19 (79)|
|Zhoushan||5·55 ± 0·27 (36)||< 0·001||Decrease||4·07 ± 0·16 (31)||< 0·001||Decrease|
|Daishan||10·82 ± 0·60 (17)||< 0·001||Increase||6·05 ± 0·33 (27)||0·005||Increase|
|Liuheng||8·10 ± 0·29 (43)||0·014||Increase||5·61 ± 0·23 (15)||0·035||Increase|
|Taohua||10·14 ± 0·72 (17)||< 0·001||Increase||5·48 ± 0·13 (32)||0·023||Increase|
|Xiashi||10·35 ± 0·65 (25)||< 0·001||Increase||6·37 ± 0·22 (9)||0·015||Increase|
|Fodu||8·44 ± 0·42 (29)||0·009||Increase||4·57 ± 0·12 (33)||0·107||ND|
|Mayi||10·86 ± 0·29 (41)||< 0·001||Increase||6·46 ± 0·30 (9)||0·011||Increase|
|Mainland||6·52 ± 0·18 (63)||4·78 ± 0·08 (36)|
|Zhoushan||6·97 ± 0·18 (41)||0·105||ND||4·61 ± 0·16 (15)||0·330||ND|
|Daishan||11·00 ± 0·34 (50)||< 0·001||Increase||7·14 ± 0·46 (5)||< 0·001||Increase|
|Liuheng||7·21 ± 0·25 (65)||0·032||Increase||5·36 ± 0·30 (8)||0·097||ND|
|Taohua||9·67 ± 0·38 (28)||< 0·001||Increase||7·04 ± 0·19 (10)||< 0·001||Increase|
|Xiashi||11·39 ± 0·34 (32)||< 0·001||Increase||7·01 ± 0·28 (16)||< 0·001||Increase|
|Fodu||8·57 ± 0·42 (25)||0·004||Increase||6·12 ± 0·34 (12)||0·002||Increase|
|Mayi||10·96 ± 0·21 (32)||< 0·001||Increase||7·70 ± 0·38 (9)||< 0·001||Increase|
variation in rice frog density, prey availability and prey size
Density of rice frogs, prey availability and prey size all varied substantially among the seven islands and the mainland in both seasons (Table 3). Compared with the breeding season, resource availability in the non-breeding season increased approximately sixfold on the mainland and fourfold (Liuheng) to 22-fold (Zhoushan) on the islands, prey size eightfold on the mainland and 0·77-fold (Xiashi) to 10-fold (Zhoushan) on the islands. Prey availability and rice frog density were significantly higher and prey size was significantly larger in the non-breeding season compared with the breeding season. This was found for both for mainland and islands combined (prey availability: t = 3·906, P = 0·006; prey size: t = 5·617, P < 0·001; frog density: t = 23·879, P < 0·001) and for islands alone (prey availability: t = 3·998, P = 0·007; prey size t = 4·820, P = 0·003; frog density: t = 20·671, P < 0·001).
|Season and location||Density (n m−1)||Prey availability (mm3 100 sweeps−1)||Prey size (mm3)|
|Mainland||0·168||253·31||14·07 ± 3·13 (36)|
|Zhoushan||0·142||152·94||11·76 ± 5·38 (13)|
|Daishan||0·242||596·09||24·84 ± 5·25 (24)|
|Liuheng||0·196||297·28||8·26 ± 1·80 (36)|
|Taohua||0·180||364·99||30·42 ± 7·72 (12)|
|Xiashi||0·238||1332·32||42·98 ± 7·24 (31)|
|Fodu||0·218||545·89||30·33 ± 19·20 (18)|
|Mayi||0·242||1147·35||29·42 ± 2·99 (39)|
|Mainland||0·390||1788·71||127·77 ± 33·25 (28)|
|Zhoushan||0·356||6152·53||130·82 ± 55·86 (47)|
|Daishan||0·488||4830·53||109·78 ± 42·88 (44)|
|Liuheng||0·416||1536·68||48·02 ± 16·44 (32)|
|Taohua||0·400||2953·40||77·72 ± 21·95 (38)|
|Xiashi||0·500||5025·19||76·14 ± 8·24 (66)|
|Fodu||0·390||7069·92||110·47 ± 13·39 (64)|
|Mayi||0·456||12746·24||179·52 ± 18·16 (71)|
Density and body size of both sexes of rice frogs in the non-breeding season were positively correlated with those in the breeding season, both for mainland and islands combined (density: r = 0·870, P = 0·005; female body size: r = 0·908, P = 0·002; male body size: r = 0·802, P = 0·017) and for islands alone (density: r = 0·862, P = 0·013; female body size: r = 0·894, P = 0·007; male body size: r = 0·811, P = 0·027).
regressions between body size of rice frogs and explanatory variables
In single regressions for the breeding season, body sizes of both male and female rice frogs were significantly and positively correlated with rice frog density for islands alone and for mainland and islands combined (Table 4). The same pattern was found in the non-breeding season, except in the case of male body size, when islands were considered on their own (Table 5). In the breeding season, male body size was also significantly and positively correlated with prey availability for mainland and islands combined and for islands alone, while female body size was related only to prey availability for mainland and islands combined (Table 4).
|Explanatory variables||Single regression (mainland and islands)||Single regression (islands alone)||Multiple regression (mainland and islands)||Multiple regression (islands alone)|
|Density||0·86 (0·007)||0·83 (0·021)||0·86 (0·007)||0·83 (0·021)|
|Prey size||0·61 (0·108)||0·69 (0·088)||−0·12 (0·753)||0·29 (0·426)|
|Prey availability||0·72 (0·044)||0·68 (0·090)||0·07 (0·859)||0·08 (0·876)|
|Ln(area)||−0·61 (0·146)||−0·08 (0·850)|
|Distance||0·47 (0·287)||0·09 (0·783)|
|Number of larger frog species||−0·40 (0·375)||−0·09(0·785)|
|Number of smaller frog species||−0·57 (0·184)||0·03 (0·950)|
|Density||0·80 (0·017)||0·79 (0·035)||0·80 (0·017)||0·79 (0·035)|
|Prey size||0·52 (0·186)||0·49 (0·262)||−0·24 (0·589)||0·02 (0·970)|
|Prey availability||0·77 (0·025)||0·76 (0·049)||0·36 (0·441)||0·36 (0·491)|
|Ln(area)||−0·50 (0·252)||0·08 (0·863)|
|Distance||0·39 (0·386)||0·02 (0·967)|
|Number of larger frog species||−0·18 (0·702)||0·15 (0·660)|
|Number of smaller frog species||−0·39 (0·392)||0·33 (0·461)|
|(c) Rice frog density|
|Prey size||0·77 (0·025)||0·61 (0·144)||0·21 (0·732)||−0·02 (0·966)|
|Prey availability||0·81 (0·014)||0·80 (0·034)||0·81 (0·014)||0·80 (0·034)|
|Ln(area)||−0·69 (0·088)||−0·24 (0·597)|
|Distance||0·48 (0·275)||0·38 (0·202)|
|Number of larger frog species||−0·392 (0·385)||−0·131 (0·704)|
|Number of smaller frog species||−0·70 (0·080)||−0·409 (0·226)|
|Explanatory variables||Single regression (mainland and islands)||Single regression (islands alone)||Multiple regression (mainland and islands)||Multiple regression (islands alone)|
|Density||0·85 (0·007)||0·86 (0·013)||0·85 (0·007)||0·86 (0·013)|
|Prey size||0·10 (0·807)||0·26 (0·596)||0·17 (0·483)||0·27 (0·291)|
|Prey availability||0·49 (0·224)||0·36 (0·426)||0·32 (0·161)||0·26 (0·301)|
|Ln(area)||−0·56 (0·192)||−0·29 (0·286)|
|Distance||0·54 (0·216)||0·05 (0·989)|
|Number of larger frog species||−0·26 (0·574)||−0·161 (0·545)|
|Number of smaller frog species||0·42 (0·355)||−0·194 (0·476)|
|Density||0·74 (0·034)||0·73 (0·063)||0·74 (0·034)||0·73 (0·063)|
|Prey size||0·11 (0·801)||0·27 (0·562)||0·18 (0·561)||0·29 (0·413)|
|Prey availability||0·52 (0·189)||0·40 (0·381)||0·36 (0·222)||0·31 (0·368)|
|Ln(area)||−0·70 (0·081)||−0·50 (0·134)|
|Distance||0·40 (0·377)||−0·09 (0·854)|
|Number of larger frog species||−0·39 (0·383)||−0·31 (0·368)|
|Number of smaller frog species||−0·61 (0·148)||−0·44 (0·390)|
|(c) Rice frog density|
|Prey size||−0·08 (0·857)||−0·02 (0·961)||−0·586 (0·397)||−0·10 (0·819)|
|Prey availability||0·21 (0·615)||0·12 (0·798)||0·21 (0·615)||0·13 (0·747)|
|Ln(area)||−0·36 (0·429)||−0·49 (0·193)|
|Distance||0·62 (0·139)||0·62 (0·139)|
|Number of larger frog species||−0·12 (0·802)||−0·41 (0·335)|
|Number of smaller frog species||−0·27 (0·552)||−0·33 (0·408)|
In multiple regressions for the breeding season, only rice frog density was significantly and positively related to body size variation in both male and female rice frogs, both for mainland and islands combined, and for islands alone (Table 4). In the non-breeding season, female body size was significantly and positively related to rice frog density both for mainland and islands combined, and for islands alone (Table 5). Female body size was also significantly and positively related to prey availability for mainland and islands combined (Table 5). Male body size was related to rice frog density for mainland and islands combined (Table 5), and there was a tendency for male body size to be positively correlated with density for islands alone (P = 0·063).
regressions between density of rice frogs and explanatory variables
In single regressions for the breeding season, rice frog density was significantly and positively related to prey availability and prey size for mainland and islands combined, and to prey availability for islands alone (Table 4). However, in multiple regression analyses, only prey availability was significantly related to rice frog density for mainland and islands combined and islands alone. In the non-breeding season, no explanatory variables were significantly related to rice frog density in either single or multiple regressions (Table 5).
In our study, the number of female rice frogs collected at each site in each season was at least 17 individuals. These sample sizes are probably large enough to overcome any potential sampling biases in observations of shifts in insular body size due to small sample size (Case & Schwaner 1993). On the other hand, body sizes of males on Mayi in both seasons, Xiashi in the breeding season, and Daishan and Liuheng in the non-breeding season were estimated from samples of only five to nine individuals, which could lead potentially to sampling bias in estimates of body size. However, gigantism of males observed on these islands in both seasons (males in Liuheng tended to be gigantic) was the same as was observed in females, suggesting that present sample sizes may adequately represent populations on these islands.
We found significant differences in body size between mainland and island populations of the rice frogs. Compared with the mainland, rice frogs were larger-bodied on all but one of the islands. This is the first report of insular shifts in body size for an amphibian. Such shifts in body size have been reported previously in mammals (Foster 1964; Lomolino 1985; Alder & Levins 1994), birds (Grant 1968; Clegg & Owens 2002; Robinson-Wolrath & Owens 2003) and reptiles (Schoener 1969, 1970; Schwaner & Sarre 1988; Case & Schwaner 1993). Our results contribute to the formation of a broad, repeatable ecological generality for shifts in body size across a range of terrestrial vertebrate taxa.
Our results showed that increases in body size of rice frogs on islands were related to increases in rice frog density. This pattern emerged in both the breeding and non-breeding seasons. An increase in rice frog density was in turn related to increases in resource availability on islands. An increase in resource availability on islands has led to higher carrying capacities, which has subsequently facilitated higher densities and individual growth rates of rice frogs (although reduced interspecific competition without change in carrying capacities can also increase population density, MacArthur, Diamond & Kar 1972). Abundant resources are less energetically expensive to acquire, because less time and energy is spent either travelling to patches of food, or in interference competition with others vying for the resources (Palkovacs 2003). Our results are also in accordance with a number of studies that have documented an increase in body size at high population densities and under conditions of high resource availability in insular populations (Case 1978; Melton 1982; Adler & Levins 1994; Hasegawa 1994; Clegg & Owens 2002). Higher densities also lead to more intense intraspecific competition among individuals in insular populations, and larger individuals are competitively superior under such conditions. At high densities, the trade off between number and size of offspring shifts to larger offspring, which favours increases in body size (Adler & Levins 1994; Palkovac 2003).
The relationship we observed between density and body size in rice frogs could be a phenotypically plastic response that represents a change in phenotype within a single generation, or it could be a longer-term evolutionary response (Stearns 1992). In view of the long isolation of about 7000–9000 years for the Zhoushan archipelago (Zhou 1987; Yiming et al. 1998), sufficient genetic variation may be available in rice frog populations on the islands for directional selection to proceed. Such directional selection is the difference in density between islands and mainland, and among islands in breeding and non-breeding seasons. Nevertheless, both phenotypic plasticity and evolutionary responses may play a role in body size shifts of the rice frog on islands. Our results again show that body size change in insular vertebrates can occur in a relatively short time span (Lister 1989; Simberloff et al. 2000).
Our findings were not consistent with the idea that either variation in prey size, or the absence of competitors, are linked to insular shifts in body size (Malmquist 1985; Schwaner & Sarre 1988; Schwaner 1990; Dayan & Simberloff 1994). We did not detect a significant correlation between prey size and body size in rice frogs in either the breeding or the non-breeding seasons. Furthermore, neither the number of larger competitor frog species nor the number of small competitor frog species were correlated with body size of rice frogs. These findings indicate that both prey size and the absence of competitors play little effect on insular shifts in body size of the rice frog.
The positive correlation between resource availability and rice frog density in the breeding season, but not in the non-breeding season, can be attributed to seasonal changes in resource availability, a common phenomenon found among insects (Janzen & Schoener 1968; Schoener & Janzen 1968; Wolda & Wong 1988). Insect abundance can change over seasons for a variety of reasons, including phenological and microclimatic changes, and variation in the availability of food resources. In the temperate zone, insects overwinter as eggs, larvae, pupae or adults (Wolda 1988), and many die before or during hibernation (Zhou 1980). Densities are usually lower in spring after hibernation, and higher in autumn following reproduction of one or several generations before preparing for hibernation. Lower food availability in the breeding season means lower carrying capacity for rice frogs, which could affect densities of rice frogs. However, food availability in the non-breeding season increased greatly so that it might be so abundant as not to be a limiting factor to rice frog densities. Dwarfism of rice frogs on Zhoushan in the breeding season but not in the non-breeding season can be attributed to seasonal changes in density and prey availability. Lower density of rice frogs and prey availability on Zhoushan in the breeding season compared with the mainland may result in decreases in body size of the rice frogs (Tables 2 and 3). In the non-breeding season, lower density on islands than the mainland could reduce body size of the frogs, while higher prey availability on the island compared with the mainland would increase the body size. As a result, no difference in the body size is found between the island and the mainland.
Observations of higher food availability on all seven islands in the breeding season and on most islands in the non-breeding season, compared with the mainland, were due possibly to the reduced number of competing species for insects on the islands (Table 2). Compared with mainland locations with a similar area, Zhoushan archipelago is species-poor in insectivorous mammals, insectivorous birds, insectivorous reptiles and amphibians (Huang 1990; Zhu 1990; Zuge 1990; Yiming et al. 1998). This has probably led to an increase in the amount of available insect food on the islands.
Dispersal ability through founder effects (Lomolino 1983) is unlikely to play a large role in insular body size shifts in rice frogs. Rice frogs cannot disperse between mainland and islands by swimming in seawater because salt water is harmful to amphibians (Gadow 1901; Yiming et al. 1998). There is some evidence that amphibians have occasionally crossed salt water by rafting, air currents and with humans (Myers 1953). Supposing that the rice frog can occasionally disperse among mainland and islands by these ways, and that larger frogs have strong dispersal ability, which has led to gigantism of rice frogs on islands, it would be expected that frogs on all islands studied would tend towards gigantism. A positive correlation between insular body size and isolation distance would also be expected. However, we did not find consistent gigantism in rice frogs on all islands (e.g. rice frogs in Zhoushan in the breeding season are dwarfs), and there was no relationship between body size and isolation distance. No association between isolation distance and insular density may be due to the fact that rice frogs could not disperse among the islands and mainland (Yiming et al. 1998). Insular density and body size were not correlated with island area probably because area is not related to density and food availability directly. Our results are consistent with a number of studies (area effect: Angerbjörn 1986; Millien 2004; isolation effect: Angerbjörn 1986; Meiri et al. 2005).
Reduced predators on islands are also suggested to be responsible for higher insular density (Heaney 1978; Smith 1992; Adler & Levins 1994; Hasegawa 1994; Palkovacs 2003). The effects of predators on insular density of the rice frog cannot be excluded from the present study. The predators of frogs on Zhoushan archipelago include small carnivores, wading birds and snakes, and species number of each of these taxa on the islands was much lower than in equivalent areas of mainland (Zuge 1990; Huang 1990; Zhu 1990). Food availability only explained a large part of variation in density in the breeding season (65·61% for mainland and island and 64·00% for island alone) (Table 4), and could not explain any variation in the no-breeding season. A reduction in predator numbers on islands could perhaps account for some of the remaining variation in population density. This idea certainly warrants further study.
We thank Y. P. Wang for assistance with the fieldwork and two reviewers for comments on the manuscript. This study was supported by the National Science Foundation (no. 30270264) and CAS Innovation Program (KSCX3-IOZ-02 and KSCX2-SW-118).
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