Assessing the Population Status of the Endangered Booroolong (Litoria booroolongensis) in Areas Subject to Non-Native Trout Stocking.

Prepared by David Hunter and Rod Pietsch

Biodiversity Conservation Section Department of Environment and Climate Change (NSW) PO Box 2115, Queanbeyan NSW 2620 Emails: [email protected] [email protected]

Unpublished Report to the NSW Department of Primary Industries

July, 2008 Trout Stocking and the Endangered Booroolong Frog

Summary

The range of the Booroolong frog (Litoria booroolongensis) has greatly contracted over the past 25 years, and as a consequence, this species is currently listed as endangered at both the State and National level. A number of factors have been suggested as contributing to this decline, including; disease caused by infection with the chytrid fungus (Batrachochytrium dendrobatidis), habitat degradation, and predation by exotic fish species. This study was contracted to assess the likely impact of trout stocking on the Booroolong frog in the South West Slopes region of . There were two primary components to this study: The first was to assess whether the Booroolong frog has persisted in areas where trout stocking has been undertaken in recent years. The second was to assess the infection status of Booroolong frog populations for the amphibian chytrid fungus, as the transport and release of fingerling trout has the capacity to spread this potentially virulent amphibian pathogen. We found Booroolong present along sections of stream immediately adjacent to, or within, areas where trout stocking currently occurs. Given the long history of trout stocking in these areas, this result suggests that Booroolong frogs are capable of persisting in the presence of trout stocking. This conclusion does not discount the possibility of more subtle impacts, or that the relative impact of stocking in the future may not increase. I also found low to moderate levels of infection with the amphibian chytrid fungus in Booroolong frog populations subject to trout stocking. While this result demonstrates that trout stocking will not introduce the amphibian chytrid fungus into areas that are free of this pathogen, there is still the possibility that stocking may spread different strains of this pathogen. If trout stocking is to continue in streams supporting populations of the Booroolong frog, then the following recommendations should be considered: 1) Monitor the persistence of Booroolong frog populations along sections of streams where trout stocking is undertaken as well as at paired sites on streams that are not stocked. 2) Undertake research to determine whether fish stocking may introduce potentially harmful strains of the amphibian chytrid fungus into Booroolong frog populations.

NSW Dept. of Environment and Climate Change Trout Stocking and the Endangered Booroolong Frog

Table of Contents:

1 Background:...... 1 1.1 Potential Impact of Non-Native Salmonid Stocking on ...... 1 1.2 Decline and Conservation of the Booroolong Frog...... 2 1.3 General Scope and Aims of this Study...... 3 2 Methods: ...... 4 2.1 Study Area and Survey Localities ...... 4 2.2 Spotlight Surveys...... 6 2.3 Habitat Measurements ...... 6 2.4 Field Swabbing for Pathogen Testing...... 6 2.5 Statistical Analysis...... 6 3 Results...... 7 3.1 Presence absence surveys and extent of potential breeding habitat...... 7 3.2 Results of swabbing for the amphibian chytrid fungus...... 8 4 Discussion...... 8 4.1 Direct Population Level Impacts of Trout Stocking...... 8 4.2 Potential for Trout Stocking to Exacerbate the Impact of the Amphibian Chytrid Fungus...... 9 4.3 Implications of these findings to the conservation management of the Booroolong frog...... 10 4.4 Summary of Specific Recommendations...... 10 5 References...... 11

Acknowledgements:

This study was funded by the Recreational Fishing Trust, NSW Department of Primary Industries. This study was covered under a NSW NPWS scientific license (No. S11409), and a NSW DECC Ethics license (No. 041025/02). Craig Watson and Cameron Westaway provided valuable advice and comments on a draft of this report. We are particularly thankful to the property owners who granted us access to undertake the surveys in this study.

NSW Dept. of Environment and Climate Change Trout Stocking and the Endangered Booroolong Frog

1 Background:

1.1 Potential Impact of Non-Native Salmonid Stocking on Amphibians. Predatory fish species can be an important factor regulating amphibian populations through predation on the eggs and tadpoles (Alford 1999). The capacity for some amphibian species to breed in aquatic environments occupied by predatory fish is typically the result of coevolution between predator (fish) and prey (tadpole) resulting in tadpole defence mechanisms to avoid being eaten by the fish (Kats et al. 1988, Sih et al. 1988, Werner and McPeek 1994). A number of experimental studies have shown that tadpole defence mechanisms are often predator or predator group specific, and may have limited effectiveness against fish species for which there has been minimal co-evolutionary history (Kats et al. 1988, Gillespie 2001). Hence, it is not surprising that the introduction of a non-native predatory fish species may result in the decline of native frog populations (Denoel et al. 2005). The release of non-native fish species may also have indirect impacts on amphibian populations. Fish predation may exclude species of amphibian from some habitats or sections of stream, resulting in greatly reduced and fragmented populations which are more prone to loss of genetic variation or local extinction (Bradford et al. 1993, Shaffer et al. 2000). Moreover, some diseases have been shown to infect both fish and amphibians and so the movement of fish to different water bodies may inadvertently result in the spread of pathogens that are harmful to amphibians (Kiesecker et al. 2001). Similarly, water used to transport fish may also contain pathogens that are harmful to amphibians, even if the fish themselves are not infected (Johnson and Speare 2003). There is also the potential for fish to compete with tadpoles for resources and so indirectly reduce their fitness (Resertarits 1995). Because of their popularity as a recreational angling species, several fish species within the family salmonidae have been extensively liberated outside their natural range. Salmonids are highly efficient predatory species, and so not surprisingly, their recent introduction into waterways in various parts of the world has been associated with the decline of native frog species (Mathews et al. 2001, Lowe and Bolger 2002, Bosch et al. 2006, Orizaola and Brana 2006). The capacity for non-native salmonids to regulate the population density of a native amphibian species was particularly well demonstrated by Vrendenburg (2004), who found that the removal of two salmonids from high altitude lakes in California resulted in the rapid recovery of Rana mucosa populations in those water bodies. While this study demonstrated a clear negative impact from the presence of introduced salmonids, it is also clear from correlative distributional studies and controlled experiments in artificial environments that susceptibility to salmonid predation may vary greatly among amphibian species (Gillespie 2001, Orizaola and Brana 2006). For over a centaury two salmonid species, brown trout, Salmo trutta, and rainbow trout, Oncorhynchus mykiss, have been widely released into rivers and dams in south- eastern Australia, and have established self-sustaining populations (McDowall 1996). Predation by introduced trout has been identified as a potential causal factor in the decline of one frog species in south-eastern Australia, the spotted tree frog, Litoria spenceri, through a combination of field observations, palatability experiments, and an in-stream experiment (Hunter and Gillespie 1999, Gillespie 2001). Since several other threatened frog species occur in streams where O. mykiss and S. trutta have become established, it has been strongly recommended that further studies examining

NSW Dept. of Environment and Climate Change 1 Trout Stocking and the Endangered Booroolong Frog the impact of introduced trout on other threatened frog fauna in south-eastern Australia be undertaken (Gillespie and Hero 1999). In addition to direct predation, the act of transporting trout and water from one catchment to another also carries the risk of spreading pathogens that may be harmful to amphibians. More specifically, the amphibian chytrid fungus (Batrachochyrium dendrobatidis), which has been identified as the primary cause of many recent frog declines along the eastern ranges of Australia (Berger et al. 1998, Skerratt et al. 2007), can be transported in water (Johnson and Speare 2003). Disease caused by this pathogen is now listed as a key threatening process (KTP) under the Commonwealth Environment Protection and Biodiversity Conservation Act 1999. One of the primary goals of the threat abatement plan for this KTP is to ‘prevent the spread of the amphibian chytrid fungus into areas where it may impact on threatened amphibian species or lead to amphibian species becoming threatened’ (DEH 2006). Hence, it is important that current trout stocking activities are assessed for their capacity to exacerbate the impact of this pathogen. It is certainly likely that ponds at Gaden Trout Hatchery are occupied by frogs that are infected with this pathogen, as a recent study found common eastern froglet ( signifera) populations in the vicinity of the hatchery to contain extremely high infection rates for this pathogen (Hunter unpublished data).

1.2 Decline and Conservation of the Booroolong Frog Included in the list of riverine frog species that have undergone recent population declines in south-eastern Australia is the Booroolong frog, Litoria booroolngensis (Gillespie and Hines 1999). Recent surveys for L. booroolongensis demonstrated that this species has declined from more than half of its historic known distribution over the past two decades (Gillespie 1999, Gillespie 2000), which formed the basis for this species being listed as endangered under the Commonwealth Environment Protection and Biodiversity Conservation Act 1999. The Booroolong Frog is also listed as endangered in New South Wales under the Threatened Species Conservation Act 1995, and as threatened in Victoria under the Flora and Fauna Guarantee Act 1988. Currently, the majority of known extant populations for L. booroolongensis exist along western flowing streams on the Southern and Central Tablelands of New South Wales, however declines in this region have also been documented and many of the persistent populations occur in very low densities along highly degraded streams (Gillespie 2000, Hunter 2007). Several factors have been proposed as contributing to the decline of L. booroolongensis, which includes habitat degradation, climate change, disease caused by infection with the amphibian chytrid fungus, Batrachochytrium dendrobatidis, and predation by introduced fish species (Gillespie and Hines 1999, Hunter 2007). A recent experimental study in artificial ponds found that both brown trout and rainbow trout prey on the tadpoles of the Booroolong frog (Hunter 2007). Hence, it is feasible to suggest that non-native trout species would be consuming the tadpoles of the Booroolong frog in the natural environment, and that this predation may result in impacts at the population level. The hypothesis that trout is negatively impacting on the Booroolong frog has important social and economic implications, as recreational trout fishing is a major industry in south-eastern Australia. Thus, adequately testing this hypothesis is important so that the management of the Booroolong frog can be implemented in a manner that meets obligations to threatened species legislation and addresses public interest for the future of trout fishing.

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1.3 General Scope and Aims of this Study. Due to possible negative impacts of exotic fish on native frogs, the strategy for stocking non-native fish species in New South Wales (NSW DPI 2005) is to have a 5km buffer zone around threatened frog records where no fish stocking will be undertaken. Due to the current distribution of the Booroolong frog on the South West Slopes of NSW, this regulation effectively precludes trout stocking from many streams where stocking has been undertaken in recent years. Because of the considerable public support for continuing trout stocking on the South West Slopes, this study was contracted by the NSW Department of Primary Industries (via the Recreational Fishing Trust) to undertake a more specific assessment of the likely impacts of trout stocking on the Booroolong frog. The specific aims of this study were to:

1). Determine the extent of suitable habitat and population persistence for the Booroolong frog in areas where non-native trout stocking is currently being undertaken.

2). Determine the presence of the amphibian chytrid fungus along streams currently subject to fish stocking.

3). Establish monitoring sites and a baseline data set for assessing the ongoing population status of the Booroolong frog in areas subject to non-native fish stocking.

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2 Methods:

2.1 Study Area and Survey Localities The study areas for this project are four streams on the South West Slopes region of New South Wales which support populations of the Booroolong frog, and which are currently subject to stocking of fingerling rainbow trout. The locality of these areas, and other streams supporting populations of the Booroolng frog on the South West Slopes, are present in Figure 1. The specific co-ordinates of the areas surveyed are presented in Table 1.

Table 1. Specific location details of sites surveyed.

Release/ Map Downstream (AMG) Upstream (AMG) Control Stream Map No. Easting Northing Easting Northing Release Gilmore Creek Tumut 8527 0605050 6086300 0605100 6085700 Control Gilmore Creek Wondalga 8527 0608300 6073700 0608200 6073000 Release Adelong Creek Tumut 8527 0698200 6087500 0698250 6086800 Control Adelong Creek Wondalga 8527 0600250 6083000 0600500 6082750 Release Goobragandra R. Lacmalac 8527 0621700 6089200 0622250 6089200 Control Goobragandra R. Blowering 8527 0629900 6081450 0629800 6080950 Release Manus Creek Ournie 8426 0589100 6029200 0589450 6029400 Control Manus Creek Ournie 8426 0588500 6024450 0588900 6024550

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Figure 1. Locality of sites on the South West Slopes where trout stocking occurs in streams supporting populations of the Booroolong frog (solid triangles), and sites where surveys were undertaken for this study (solid circles). Highlighted sections of stream are sections of stream known to support populations of the Booroolong frog.

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2.2 Spotlight Surveys

Surveys for the Booroolong frog were undertaken at night by spotlighting for eye- shine along the stream transects. This was undertaken by walking upstream and spotlighting along all emergent areas of the stream to within four meters of the waters edge. Surveys also involved spotlighting for tadpoles within the stream around bedrock and cobble bank structures where breeding may have occurred. Frogs were only hand-captured if their identification required confirmation, or if chytrid swabbing was undertaken. Frogs were handled wearing a new pair of disposable rubber gloves, which were disposed of immediately after the release of the frog. Frogs were typically handled for less than 30 seconds.

2.3 Habitat Measurements The number and length of potential rocky breeding areas along the stream transect was quantified by measuring all sections of stream bank that consisted of a continuous cover of loose rock or bedrock for greater than one meter.

2.4 Field Swabbing for Pathogen Testing The swabbing procedure involved holding the frog by the back legs and wiping the frog with a sterile swab three times on each of the feet, hands, inside and outside of the thighs, and stomach and back region. The swabs were stored in a cool location (esky with ice and then fridge) until delivery to the CSIRO Animal Health Laboratory in Geelong, where they were then screened for the presence of the amphibian chytrid fungus DNA. This was undertaken using Taqman real-time PCR assay (see Boyle et al. (2004) and Hyatt et al. (2007) for details of this procedure).

2.5 Statistical Analysis Uncertainty around the total proportion of adults testing positive for infection with the amphibian chytrid fungus was estimated using a Bayesian approach with uninformative priors. The 95% credible intervals were propagated using Markov Chain Monte Carlo methods with 100,000 samples after the first 10,000 samples were discarded. This was undertaken using the WinBUGS software package, version 1.4 (Spiegelhalter et al. 2003).

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3 Results

3.1 Presence absence surveys and extent of potential breeding habitat. The Booroolong frog was detected along all section of stream surveyed (Table 1). The number of individuals detected varied within and among streams surveyed, with there generally being more frogs detected along sections of stream away from the stocking areas (control), than was detected at the stocking sites (release) (Table 2).

Table 2. Number of Booroolong frogs detected and extent of potential breeding habitat along sections of stream surveyed in this study.

Release/ No. No. Number of Number of Total Frogs Frogs Breeding Breeding Length of Control 1st 2nd Areas Areas Breeding Stream Census Census Occupied Available Habitat Release Gilmore Creek 4 2 2 5 27 meters Control Gilmore Creek 6 8 3 7 42 meters Release Adelong Creek 6 - 2 3 18 meters Control Adelong Creek 7 9 5 9 57 meters Release Goobragandra R. 18 15 4 11 146 meters Control Goobragandra R. 26 34 5 17 178 meters Release Manus Creek 9 6 3 10 38 meters Control Manus Creek 8 12 2 7 64 meters

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3.2 Results of swabbing for the amphibian chytrid fungus. The amphibian chytrid fungus was detected along all streams sampled in this study (Table 3). While there was considerable variation in the proportion of individuals testing positive for infection among steams, there was overlap in the 95% credible intervals indicating that the variation wasn’t significant (Table 3).

Table 3. Results for the screening of Booroolong frog populations for infection with the amphibian chytrid fungus.

Stream No. No. Testing Proportion 95% Credible Samples Positive Testing Positive Intervals

Gilmore Creek 9 1 0.11 0.02 – 0.42

Adelong Creek 11 6 0.54 0.23 – 0.76

Brungle Creek 16 3 0.19 0.07 – 0.47

Goobragandra River 10 2 0.20 0.08 – 0.51

Coppabella Creek 10 3 0.30 0.04 – 0.61

4 Discussion

4.1 Direct Population Level Impacts of Trout Stocking. Given the presence of the Booroolong frog at all sites surveyed, it appears that predation or competition resulting from the stocking of trout at these sites does not displace this species. This statement is made with much caution, as the present study does not have sufficient data to assess impacts that are more subtle, or that may manifest over a longer period. In any case, several factors suggest that impacts from trout stocking may not be of immediate concern for the Booroolong frog populations in question. These include: - The presence of trout in these streams is not dependant on the stocking program, and the stocking of trout may not greatly increase the resident trout population along the entire stream. - The Booroolong frog populations where trout stocking is undertaken each occupy greater than 20 kilometers of stream, and so local impacts of trout stocking are unlikely to have a significant impact at the broader population/stream level. In the case of the Goobragandra River, there are significant barriers to trout movement upstream of the stocking site. - Other processes threatening the viability of the Booroolong frog in Gilmore Creek, Adelong Creek and Manus Creek (habitat degradation and stream drying during

NSW Dept. of Environment and Climate Change 8 Trout Stocking and the Endangered Booroolong Frog drought events, Hunter and Smith 2006) would also be reducing the effectiveness of trout stocking in those streams. One observation in the data that may suggest an impact of trout stocking was that the abundance of the Booroolong frog was greater at the sites furthest away from stocking (Table 2). This assumes that the observed abundance reflects actual abundance, which may not be the case. Even if the observed pattern of abundance did reflect the real situation, this pattern could also be explained by the variation in extent of available breeding habitat, rather than localized effects from trout stocking. This is because the sites surveyed closer to stocking areas also had less available breeding habitat (Table 2). Moreover, Booroolong frog populations have the capacity to fluctuate greatly in abundance from one year to the next (Hunter 2007), which limits the capacity to one year of relative abundance data. In any case, the reality of this study is that definitive statements about the impact of trout stocking on the Booroolong frog could only be made if the impacts where sufficient to completely displace this species from sections of stream in close proximity to the stocking areas. With regards to further research, it is worth mentioning that assessing population level effects of trout stocking on the Booroolong frog is greatly complicated by two important issues. The first is that there is already a resident population of both brown and rainbow trout in the streams where trout stocking is occurring. Hence, the question of interest is; does trout stocking exacerbate the impact of trout in those streams. The second complicating factor is that there are other exotic fish species present in those streams (mosquito fish, redfin perch and carp) that have also been identified as predators of Booroolong frog tadpoles (Hunter 2007). As such, it would be necessary to identify whether releasing fingerling trout in those streams increases the overall impact of exotic fish on the Booroolong frog. It may be extremely difficult, or effectively impossible, to adequately determine whether there are additional impacts from trout stocking, particularly given that other environmental factors may strongly influence interactions among the different exotic fish species currently present.

4.2 Potential for Trout Stocking to Exacerbate the Impact of the Amphibian Chytrid Fungus. We identified the presence of the amphibian chytrid fungus in extant Booroolong frog populations where trout stocking is being undertaken (Table 3). This result is not surprising as these populations are connected to populations of other frog species that are likely to act as vectors for this pathogen. This result is also consistent with the findings of Kriger (et al. 2007), who found the amphibian chytrid fungus present throughout populations of Lesueur’s frog (Litoria lesueuri), a sister species to the Booroolong frog. The extent to which the amphibian chytrid fungus is contributing to the regulation of extant Booroolong frog populations on the South West Slopes is unknown. It is certainly possible that this pathogen is highly virulent to the Booroolong frog, and that any action increasing rates of infection among individuals could negatively impact on this species. In any case, it is unlikely that the action of stocking trout in these streams would greatly increase infection rates in the resident Booroolong frog population. One potentially important issue not examined in this study is that fish stocking may spread a different, more virulent strain of the amphibian chytrid fungus into Booroolong frog populations. Different strains of the amphibian chytrid fungus, whose virulence varies significantly, have been identified from different geographic localities (Berger et al. 2005, Retallick and Miera 2007). Hence, it is certainly NSW Dept. of Environment and Climate Change 9 Trout Stocking and the Endangered Booroolong Frog possible that the population of the amphibian chytrid fungus in the vicinity of the Gaden Trout Hatchery is epidemiologically different to that currently present in Booroolong frog populations on the South West Slopes. Therefore, with our current knowledge, it can not be discounted that trout stocking will exacerbate the impact of the amphibian chytrid fungus on Booroolong frog populations through spreading different strains of this pathogen.

4.3 Implications of these findings to the conservation management of the Booroolong frog. Trout stocking on its own does not appear to pose a significant threat to the persistence of Booroolong frog populations on the South West Slopes. However, it is just one of a suite of potentially threatening factors that are operating in the ecosystem and the synergistic effects of these factors are not known. Therefore, monitoring and adaptive management are important for detecting and reacting to any processes negatively impacting on this species. With respect to investigating whether negative impacts are occurring, the burden of proof should lie with demonstrating that there is no impact, rather than there is! Hence, if it has not been adequately demonstrated that there is no impact, the precautionary principle should be applied if there is a reasonable probability of suggesting no impact when there actually is, particularly if the resulting level of impact could significantly harm the viability of this endangered frog. Based on the issues discussed in section 4.1, it seems reasonable to conclude that current trout stocking activities are unlikely to significantly increase the impact of predation or competition from non-native fish on the Booroolong frog, and that any increased impacts are likely to be relatively localized. This may change depending on the status of the populations in question, and so monitoring the persistence of these populations should be undertaken if trout stocking continues. A potentially more problematic issue is whether trout stocking may increase impacts from the amphibian chytrid fungus through spreading more virulent strains of this pathogen. Wheter this is likely cannot be assessed based on current information. However, given the potential for this pathogen to devastate amphibian populations (Sherratts et al. 2007), it should not be dismissed. If trout stocking is going to continue in streams where the Booroolong frog occurs, then specific research testing the sensitivity of this species to local isolates of the amphibian chytrid fungus should be undertaken.

4.4 Summary of Specific Recommendations. 1) Monitor the persistence of Booroolong frog populations along sections of streams where trout stocking is undertaken as well as at paired sites on streams that are not stocked. 2) Undertake research to determine whether fish stocking may introduce potentially harmful strains of the amphibian chytrid fungus into Booroolong frog populations.

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5 References

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Gillespie, G. R. and Hines, H. B. (1999). Status of Temperate Riverine Frogs in South-eastern Australia. In: A. Campbell (Ed.) Declines and Disappearances of Australian Frogs. Environment Australia, Canberra, pp. 109-130. Hunter, D. (2007). Conservation management of two threatened frog species in south- eastern New South Wales, Australia. Unpublished PhD Thesis, University of Canberra. Hunter, D. and Gillespie, G. R. (1999). The distribution, abundance and conservation status of riverine frogs in Kosciuszko National Park. Australian Zoologist, 31: 198-209. Hyatt, A. D., Boyle, D. G., Olsen, V., Boyle, D. B., Berger, L., Obendorf, D., Dalton, A., Kriger, K., Hero, M., Hines, H., Phillott, R., Campbell, R., Marantelli, G., Gleason, F. and Colling, A. (2007). Diagnostic assays and sampling protocols for the detection of Batrachochytrium dendrobatidis. Diseases of Aquatic Organisms, 73: 175-192. Johnson, M. L. and Speare, R. (2003). Survival of Batrachochytrium dendrobatidis in water: Quarantine and disease control implications. Emerging Infectious Diseases, 9: 922-925. Kats, L. B., Petrana, J. W. and Sih, A. (1988). Antipredator defenvces and the persistence of amphibian larvae with fishes. Ecology, 69: 1865-1870. Kiesecker, J. M., Blaustein, A. R. and Miller, C. L. (2001). Transfer of a pathogen from fish to amphibians. Conservation Biology, 15: 1064-1070. Lowe, W. H. and Bolger, D. T. (2002). Local and landscape-scale predictors of salamander abundance in New Hampshire headwater streams. Conservation Biology. 16: 183-193. Mathews, K. R., Pope, K. L., Preisler, H. K. and Knapp, R. A. (2001). Effects of nonnative trout on Pacific treefrog (Hyla regilla) in the Sierra Nevada. Copeia 2001: 1130-1137. McDowall, R. M. (ed) (1996). ‘Freshwater Fishes of South-eastern Australia. 2nd edition’. (Reed, Sydney). NSW DPI (2005). The NSW Freshwater Fish Stocking Fisheries Management Strategy. ISBN No. 0 7310 9431 X. Orizaola, G. and Brana, F. (2006). Effect of salmonid introduction and other environmental characteristics on amphibian distribution and abundance in mountain lakes of northern Spain. Animal Conservation, 9: 171-178. Resetarits, W. J. (1995). Competitive asymmetry and coexistence in size structured populations of brook trout and spring salamanders. Oikos, 73: 188-198. Retallick, R. W. R. and Miera, V. (2007). Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Diseases of Aquatic Organisms, 75: 201-207. Shaffer, B. H., Fellers, G. M., Magee, A. and Voss, R. (2000). The genetics of amphibian declines: population substructure and molecular differentiation in the Yosemite Toad, Bufo canorus (Anura, Bufonidae) based on single-strand conformation polymorphism analysis (SSCP) and mitochondrial DNA sequence data. Molecular Ecology, 9: 245-257.

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Sih, A., Petranka, W. and Kats, L. B. (1988). The dynamics of prey refuge use: a model and test with sunfish and salamander larvae. American Naturalist, 132: 463-483. Skerratt, L. F., Berger, L., Speare, R., Cashins, S., McDonald, K. R., Phillott, A. D., Hines, H. B. and Kenyon, N. (2007). Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth, 4: 125-134. Spiegelhalter, D. J., Thomas, A., Best, N. G. and Lunn, D. (2003). WinBUGS version 1.4 user manual. Medical Research Council Biostatistics Unit, London, England. Vredenburg, V. T. (2004). Reversing introduced species effects: Experimental removal of introduced fish leads to rapid recovery of a declining frog. Proceedings of the National Academy of Sciences, 101: 7646-7650. Werner, E. E. and McPeek, M. A. (1994). Direct and indirect effects of predators on two anuran species along an environmental gradient. Ecology, 75: 1368-1382.

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