Competition between the larvae of the introduced cane toad Bufo marinus (Anura: Bufonidae) and native anurans from the Darling Downs area of southern Queensland

INTRODUCTION

Human-assisted introductions of species are a feature of ecosystems world wide. While it is difficult to make general predictions about the success or impact of invading species, many studies have demonstrated an impact of particular invading species ( Lodge 1993). Predation and habitat alteration by invading species are seen as the most important mechanisms of impact on native species, although competitive impact may be underestimated ( Lodge 1993).

In Australia the introduced cane toad, Bufo marinus, is still undergoing range expansion ( Covacevich & Archer 1975; Van Beurden & Grigg 1980; Easteal et al. 1985 ; Freeland & Martin 1985; Seabrook 1991), and its impact on native fauna is still largely unquantified (but see Freeland & Kerin 1988; Alford et al. 1995 ; Crossland 1997; Crossland & Alford 1998). Although the toad’s spread and impact in northern Australia has been investigated ( Alford et al. 1995 ) little attention has been paid to its potential spread westward and southward via the Darling River catchment in southern Queensland and its potential impact on the native species of this region. Movement down rivers is probably much greater than across drainage systems ( Freeland & Martin 1985). The potential downstream spread into areas of New South Wales, Victoria and South Australia ( Sutherst et al. 1996 ) suggests a need for base-line biological and ecological data on the cane toad at the edge of its current range in the Darling River catchment area of southern Queensland.

Bufo marinus was first recorded on the Darling Downs (in the headwaters of the Darling River system) more than 25 years ago ( Floyd et al. 1981 ) and the species currently occupies a small area around and to the north of Chinchilla on the northern Darling Downs ( Clerke 1996). Clerke (1996) collected basic ecological data for B. marinus in this area. His data indicate that, while B. marinus has a well established and expanding population in the northern Darling Downs, adult densities in the area are much lower than in coastal sites at similar latitude and at sites in northern Australia. Although adult densities are low, high densities of larvae and metamorphs occur at some sites. Therefore, B. marinus may still be affecting populations of native anurans because high densities of B. marinus larvae and metamorphs are added to habitats normally containing only the larvae and metamorphs of native anurans.

There have been many studies of interspecific competition in anuran larvae (see Alford, 1999 for review). These studies indicate that interspecific interactions between larvae have the potential to influence distributions of species (e.g. Odendaal & Bull 1983). Bufonid larvae have been shown to affect growth and development of other anuran species negatively (e.g. Wilbur & Alford 1985), and Alford (1999) has suggested that B. marinus larvae are aggressive while feeding, a trait that may provide a competitive advantage. Although there has been concern that B. marinus may have a negative impact on larvae of native anurans, particularly in terms of their high densities relative to native species ( van Beurden 1980), there have been few studies of competition between larvae of B. marinus and native anurans ( Crossland 1997; Alford 1999). The work reported here is a preliminary assessment of the impact of cane toad larvae on the survival and growth of the larvae of selected native species of anurans that co-occur with B. marinus on the Darling Downs region of southern Queensland.

METHODS

METHODS

Two types of larval competition trials were conducted: in artificial water bodies and in natural water bodies using enclosures. Small wading pools (1.4 × 1.2 × 0.2 m) were used as artificial ponds. For each of the artificial water body experiments, 30 pools were placed in five rows of six pools on level ground approximately 600 m from the nearest water body (Cutthroat Creek) in the Barakula Forestry settlement. Pools were filled to a depth of 20 cm (i.e. 300–350 L) with creek water filtered through 1-mm mesh netting. Creek water was turbid and, after filling, pools contained a layer of fine sediment. The first two trials were conducted with the pools uncovered, allowing rapid immigration of a range of mobile aquatic organisms, including predators (e.g. odonates, hemipterans and dytiscids). For remaining experiments, pools were covered with 50%-shade cloth which generally prevented colonization by these predators. Water was replaced between experimental trials.

Enclosures were constructed from fibreglass flywire mesh fastened to wooden stakes and measured 1.0 × 0.5 × 0.4 m. Enclosures were fixed in place by the stakes at the edge of a small man-made dam so they enclosed approximately 100 L of water. For each of these enclosure experiments, five blocks of six enclosures were distributed around the margin of the dam.

The mechanical diallel design for examining competition between two species ( Underwood 1986) was used in all trials. The four treatments used in the design were: 50 Bufo alone, 50 Bufo plus 50 native, 100 Bufo plus 50 native, and 50 native alone. There were five replicates of each treatment in all trials. The higher density Bufo treatment (i.e. 100 Bufo plus 50 native) was included in the assessment of B. marinus impacts because B. marinus often occur at higher densities relative to native species.

Individual species were also grown at a density of 100 per pool/enclosure to check their response to increased density in these experimental conditions. However, because the main focus of the study was to examine interspecific competition, these data were not used here, except for one wading pool trial where mortality rates were so high that the data were incorporated into an ‘alone’ versus ‘mixed’ comparison (see RESULTS). The resultant densities for each species ranged from 0.17 to 0.33 larvae L^–1 in wading pools and 0.5–1.0 larvae L^–1 in enclosures which falls within the range of observed natural densities of the species examined ( Alford et al., 1995 , personal observation).

Bufo marinus on the Darling Downs breed from September to March ( Clerke 1996) and their breeding pulses coincide with a number of native anuran species. Although 21 native anuran species occur in the area ( Mason 1988), many with predominantly southern distributions covering the Murray–Darling catchment (e.g. Limnodynastes fletcheri, Notaden bennetti) ( Cogger 1992; Barker et al. 1995 ), trials were restricted to those species for which eggs and or larvae were available in sufficient numbers for experimentation. Focus was also directed towards myobatrachid species rather than hylids, because myobatrachid and bufonid larvae tend to be substrate feeders and are therefore more likely to interact with each other than with hylid larvae which are predominantly mid-water feeders ( Altig & Johnston 1989).

Five wading pool trials and two enclosure trials were conducted over the periods 31 November 1994 to 28 February 1995, and 31 October to 19 December 1995. Details of the species used in the different trials are shown in Table 1. All individuals were collected either as eggs or as larvae from the Barakula State Forest and surrounding grazing land.

Although timing and size at metamorphosis are the best indicators of performance during the larval phase, these measures could not always be recorded due to disturbance to enclosures (e.g. trampling by livestock, crayfish tearing enclosures, other anurans laying eggs in enclosures). Therefore, survival and length at set times (6–25 days) prior to disturbances were used as measures of performance. Growth and development were monitored by taking a random sample of 10 individuals of each species from each pool, recording their developmental stage ( Gosner 1960) and measuring their total length to the nearest 0.5 mm by placing them in a Petri dish held over 0.5-mm-grid graph paper. The mean size of this sample of 10 tadpoles was taken as an estimate of mean size of tadpoles in each pool and was used as the estimate of growth rate in subsequent statistical analyses. Survival was generally checked once per trial by dip-netting the pools until no individuals were captured. All survival estimates were converted to finite survival rates per day ( Krebs 1989).

To assess the amount of overlap in pond use between B. marinus and native species, 30 water bodies were visited once per week from January to March 1995. Water bodies sampled were within easy access to forestry roads and were selected to include a range of water body types (creeks/rivers, dams, gutters and claypan pools). The presence of eggs and larvae were noted in each water body and any unidentified specimens were returned to the laboratory where they were grown to a stage where they could be identified (late-stage larvae or metamorphs). Margins of water bodies were also searched for metamorphs and adults. In addition, a number of these sites were visited between 19.00 and 21.00 hours to record species calling, either directly or by leaving a small cassette recorder at a site for approximately 10 min, the species being identified later from the taped calls.

RESULTS

Four species whose clutch laying coincided with B. marinus were examined: Limnodynastes tasmaniensis in two wading pool and two enclosure trials, and Limnodynastes ornatus, Limnodynastes terraereginae and N. bennetti each in one wading pool trial ( Table 1). Table 2 shows the mean daily survival rate for larvae in all treatments and Table 3 shows mean sizes. Survival rates varied considerably between trials and sometimes within trials (overall range 0.98–0.36 per day for Bufo; 0.98–0.17 per day for native species). Ranges of mortality rates were similar in wading pools and enclosures despite the differences in density and growth conditions. Lowest survival occurred in the trial with N. bennetti.

The presence of Bufo had a significant negative effect on survival of Limnodynastes tasmaniensis (one of two wading pool trials but not in two enclosure trials) and L. terraereginae (one of one wading pool trial) but not on L. ornatus or N. bennetti. Bufo had a significant negative effect on the growth of all species except L. ornatus. Bufo survival was not affected by the presence of any of the four native species and growth was negatively affected by L. tasmaniensis in one enclosure trial but positively affected by the same species in one wading pool trial ( Table 3).

DISCUSSION

Many studies have demonstrated interspecific competition between anuran larvae (see Alford 1999). Although it has been claimed that larvae of the introduced cane toad might compete with native anuran larvae, there are few studies of this interaction (e.g. Crossland 1997; Alford 1999), and no studies of the interaction in the southern part of the B. marinus range.

The results of the larval competition experiments reported here indicate that while there was no consistent evidence that B. marinus larvae were negatively affected by native species, there was evidence that B. marinus can affect the growth of native anurans under some circumstances. Three of the four species examined showed a reduced growth rate in the presence of B. marinus. An assessment of the competitive effect of B. marinus on the remaining species, L. ornatus, was not possible because of reduced densities of L. ornatus in mixed pools. However L. ornatus is an aggressive and active tadpole and previous studies have indicated that it is not affected by B. marinus ( Alford 1999), although late arriving L. ornatus may be out-competed by earlier arriving B. marinus larvae ( Crossland 1997).

Evidence of a negative interaction in enclosure trials was less conclusive even though these trials were conducted at a higher density than the wading pool experiments. Although growth of B. marinus and natives in wading pools appeared to match growth rates of similar larvae in natural ponds, growth in enclosures was faster than in wading pools. This suggests that food resources may be important in determining the outcome of interactions between B. marinus and the species examined. The mechanism of the competition (exploitation or interference competition) between the species was not examined in this study.

Clearly, further experimentation is needed to determine whether competition is likely to occur in natural water bodies. Although wading pools offer more control, enclosure experiments may provide a more realistic indication of the interaction between species. These enclosure experiments would need to be conducted in the full range of water body types in which B. marinus interacts with native species.

This study provides only limited evidence for an impact of B. marinus on the survival of the larvae of native anurans. Bufo marinus reduced survival of L. terraereginae in the only trial with that species, while reduced survival of L. tasmaniensis occurred in only one of four trials. Bufo marinus might cause reduced survival of native species by competitive interactions, predation, or toxic effects ( Crossland & Alford 1998; Crossland 1998). The causes of the lower survival of native species in some trials was not clear. Predation by B. marinus was a possible cause in the trial where L. tasmaniensis survival was reduced, because that trial involved recently hatched L. tasmaniensis grown with larger, later stage B. marinus. However, Crossland (1998) has found that B. marinus are unlikely to have a large impact as predators of native larvae. The more consistent negative impact of B. marinus in the growth rate trials in this study suggests that reductions in survival caused by reduced growth rates (i.e. through increased risk of predation or desiccation) might be more important than the impact of B. marinus as a predator.

However, mortality of larvae of native species resulting from their predation of B. marinus eggs and hatchlings may have a larger impact on native anurans than either competition with, or predation by, B. marinus (see Crossland & Alford 1998). High mortality in a cohort of large, developmentally advanced tadpoles may have more impact on the number of individuals metamorphosing and, therefore, on adult population size, than reduced growth rates occurring in the early stages of larval development. The impact of predation of B. marinus larvae by larvae of native species was not investigated in this study, although observations of dead, developmentally advanced larvae of native species in pools with new cohorts of B. marinus larvae have been made in the study area (Williamson, personal observation, 199?).

In anurans, population size may be determined by factors occurring in the aquatic phase, the terrestrial phase, or both ( Wilbur 1980). The data on pond use by B. marinus indicated that most native species are found in a high proportion of sites that do not contain B. marinus. This probably reflects the low density of B. marinus adults in this region ( Clerke 1996) relative to many of the native species. Therefore, although high densities of B. marinus larvae occur at some sites, larval populations of native species may not be affected greatly because most native species use a larger number of breeding sites than B. marinus and are therefore likely to escape interactions with B. marinus. Bufo marinus might also be having minimal impact on those native anuran species whose population sizes are determined by factors occurring in the terrestrial phase of the life-cycle because most species still produce sufficient numbers of recruits from the ponds where B. marinus do not breed to maintain the adult population size.

These data on the overlap of pool use were based on observations of adults as well as metamorphs, larvae and eggs. Adults may be present at a water body without using it for egg laying, and breeding success for native species may vary between water bodies. Therefore, a more detailed study of the overlap of breeding use of water bodies, and the relative breeding success from different water bodies, is needed before firm conclusions can be drawn about whether the low overlap translates to low impact on native species. For example, B. marinus may have higher impact if the water bodies that it does use are sites of high recruitment for native species.

This brief study suggests that B. marinus could negatively affect the growth and survival of native anurans of the Murray–Darling catchment. However, if population densities of B. marinus remain low then their impact on populations of native anurans by way of competition may be minimal because there will always be a high proportion of breeding sites where native anurans can breed in the absence of B. marinus. However, the exact extent of the impact of B. marinus will not be clear without a more detailed study of the interactions between B. marinus and all the native anuran species occurring in the Murray–Darling catchment, and the role that the larval phase plays in influencing adult population sizes of these native species.

Acknowledgements

The study was funded by the CSIRO Cane Toad Research Committee.

I thank Murray Sharman, David Ramsey and Randall Storey (from where?) for excellent research assistance; John Schultz and Darryl Bailey at the Barakula Forest Office for providing space, water and accommodation; Allan Greer (from where?) for allowing collection of frogs from his property; Greg Czechura (Queensland Museum) for helping with frog identification; Robert Clerke (from where?) for finding out where the toads were in the first place; and Michael Crossland (from where?) for providing valuable comments on an earlier draft of this manuscript.