Bullfrog invasion of a California river: the role of larval competition - Rana catesbeiana

Ecology, Sept, 1997 by Sarah J. Kupferberg

INTRODUCTION

Biological invasion poses a serious threat to freshwater biodiversity (Allan and Flecker 1993). Invasions have been implicated in 68% of the forty North American fish extinctions that have occurred since the turn of the century (Miller et al. 1989). A high proportion of endemic aquatic animals are at risk relative to terrestrial fauna (Master 1990). Amphibians are of particular concern because of their apparent global population declines (Blaustein and Wake 1990, Wake 1991), their sensitivity to a wide array of environmental stressors (Harte and Hoffman 1989, Carey 1993, Pounds and Crump 1994, Blaustein et al. 1994a), and their susceptibility to local and global extinctions (Blaustein et al. 1994b).

Declines of native ranid frogs in western North America have coincided with introductions and subsequent range expansions of the bullfrog, Rana catesbeiana (Moyle 1973, Bury and Luckenbach 1976, Green 1978, Hammerson 1982, Clarkson and DeVos 1986, Clarkson and Rorabaugh 1989). Bullfrogs, although native to North America, are alien west of the Rocky Mountains (Stebbins 1985). They have been introduced around the world, including Europe (Albertini and Lanza 1987, Stumpel 1992), South America, and Asia (M. J. Lannoo, unpublished report, Declining Amphibian Task Force, IUCN). In California, bullfrogs were first introduced in 1896 (Heard 1904) for human food after populations of native frogs, particularly Rana aurora, the red-legged frog, were overharvested (Jennings and Hayes 1985). The role of bullfrogs in native ranid declines is unclear because there have often been concurrent alterations of aquatic habitats, changes in land use of adjacent terrestrial habitats, and introduction of non-native fishes (Hayes and Jennings 1986), which can devastate populations by predation on tadpoles (Bradford 1989, Bradford et al. 1993).

I studied bullfrog impacts in a watershed where invasion has only recently occurred and which remains relatively pristine. Here I present observations that where bullfrogs are well established in otherwise unaltered river habitats, breeding populations of the native ranid are much lower than populations upstream of the invasion front. I also present experimental evidence that bullfrog tadpoles have negative impacts on native frogs. To determine what role larval competition may play in the exclusion of native frogs by bullfrogs, I investigated: (1) The relative competitive abilities of different size classes of native and invading tadpoles; (2) The impact of bullfrogs on native frogs and algal food resources in larger enclosures in the natural river; and, (3) The potential role of chemical interference or feces-borne pathogens as mechanisms of competition.

NATURAL HISTORY AND STUDY SYSTEM

This research was conducted in two rivers at the Angelo Coast Range Reserve, Mendocino Co., California (39 [degrees] 44[minutes] N, 123 [degrees]39 [minutes] W) [ILLUSTRATION FOR FIGURE 1 OMITTED]. The watershed of the South Fork Eel River is sparsely populated by humans and is dominated by mixed coniferous forest and oak-madrone woodland. Ten Mile Creek, a tributary of similar drainage area, flows through grazed pastures. Stock ponds and recreational fishing ponds along these rivers are possible sources of invading bullfrogs, which began to appear on the reserve coincident with a multi-year drought in the late 1980s (Kupferberg 1996a). The native anurans include the foothill yellow-legged frog, Rana boylii, a California Species of Special Concern (Jennings and Hayes 1994) and the Pacific treefrog, Hyla regilla.

I investigated larval competition rather than predation by adult bullfrogs (Moyle 1973) because adults did not exhibit the same degree of habitat and resource overlap as larvae. R. boylii commonly occurred along shaded steep gradient tributaries and Hyla were widely dispersed throughout the forests and meadows of the surrounding watershed, habitats not used by bullfrogs. Gut contents of adult and juvenile bullfrogs collected on site did not include native frogs (C. Bailey, unpublished data). All three species were found to use the main stem South Fork Eel River and Ten Mile Creek to breed. Larval competition was suggested because feces of the three tadpole species contained similar diatoms, algae, and detritus.

As is typical for rivers experiencing the winter flood-summer drought hydrologic conditions of a mediterranean climate, algal blooms occurred in the late spring when discharge declined and the rock bedded river was clear and sunlit. In this system the dominant alga is Cladophora glomerata, a periphytic filamentous green alga. The growth of Cladophora turfs on rock substrates is controlled by both hydrologic and trophic conditions including limited nitrogen availability (Power 1992a). When Cladophora is overgrown by taxa not susceptible to nitrogen limitation, such as the cyanobacteria Nostoc and diatoms in the genus Epithemia, the algae slough off and float to the surface. The abundance of floating algae therefore indicates tadpole food quality. The epiphytes can completely cover the filaments of host algae, and tadpoles can effectively remove diatoms from Cladophora (Kupferberg 1997). Diatoms increase the nutritional value of Cladophora because the most common epiphytes, Epithemia spp., contain nitrogen fixing cyanobacterial endosymbionts. The protein content of Cladophora with epiphytes is 11.3% of dry mass vs. 5.8% without (Kupferberg et al. 1994). In addition, epiphytes store excess photosynthate as lipid rather than carbohydrate so Cladophora with epiphytes has higher fat than Cladophora without epiphytes. Hyla regilla (Kupferberg et al. 1994) and R. boylii (Kupferberg 1996a) tadpoles fed diets rich in diatoms had enhanced growth, development, and survival to metamorphosis.