Batrachomyia strigapes (Diptera) Parasitism of Uperoleia laevigata (Anura)

Batrachomyia strigapes (Diptera) Parasitism of Uperoleia laevigata (Anura) Author(s): C. B. Schell and Shelley Burgin Source: The Journal of Parasitology, Vol. 87, No. 5 (Oct., 2001), pp. 1215-1216 Published by: Allen Press on behalf of The American Society of Parasitologists Stable URL: http://www.jstor.org/stable/3285273 Accessed: 03-09-2015 07:44 UTC

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RESEARCH NOTES 1215

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Batrachomyiastrigapes (Diptera)Parasitism of Uperoleialaevigata (Anura) C. B. Schell and Shelley Burgin*,Centrefor Landscape and Ecosystems Management,Locked Bag 1797, South PenrithDistributionCentre, Australia,1797. ABSTRACT: To quantify the occurrence of the dipteran parasite Batra-

chomyia strigapes, the ground frog assemblage associated with a large ephemeral wetland in Western Sydney was sampled between January 1999 and April 2000. Parasite infection was restricted to Uperoleia laevigata (5.1%, n = 1,492). Parasites were found under the parotoid glands, most frequently on the left side. After correction for frog size, infection was shown to significantly reduce frog weight. Despite reduced individual fitness, because the level of infection was low in the population, it is unlikely to have a major effect on the anuran population under current environmental conditions. There is a paucity of data on parasitism of Australian anurans. Most published accounts are restricted to helminths (Barton and Richards, 1996; Barton, 1999) and parasitism associated with amphibian disease (Laurance et al., 1996; Berger et al., 1997; Hero and Gillespie, 1997; Berger and Spear, 1998). However, species of the dipteran Batrachomyia have been reported to parasitize frogs with larvae living in the subcutaneous lymph spaces. To respire, the parasites project their spiracles through a break in the host's skin and procure nourishment from the host's blood vessels (McAlpine, 1955). Batrachomyia spp., first described from an adult fly collected in Tasmania (Malloch, 1927), generally display marked host specificity. However, Batrachomyia strigapes has been recorded from two anuran species (Uperoleia mormorata and Pseudophryne bibronii; McAlpine, 1955) with prominent parotoid glands, and we observed them parasitizing Uperoleia laevigata in western Sydney. It was this observation that prompted us to determine the prevalence of B. strigapes within a frog community and assess its effect on frog fitness. The ground frog (Myobatrachidae) assemblage associated with a large ephemeral wetland (0.125 km2) on the Richmond campus of the University of Western Sydney (6278375N, 288375E) was sampled monthly between January 1999 and April 2000. The area is characterized by warm, wet summers and cool, dry winters, and the soil consists of clays and silts (Benson and Howell, 1990), resulting in frequent flooding during wet periods. Maximum water depth for the study area was 0.38 m, although levels of 0.10 m were more common. Sampling was based on a stratified random sampling regime. The perimeter of the wetland was divided into 6 segments, representing grassland, woodland, and sclerophyllous vegetation types. In each segment, 3 separate arrays of drift fence and associated pitfall traps were *To whom correspondence should be addressed.

installed (Heyer et al., 1994). Each segment of the flywire drift fence consisted of 3 drift fences, 5 m long by 0.4 m high, arranged in a Yconfiguration. Each array had a central pitfall trap, as did the terminal end of each arm of the Y-configuration. Traps were opened for 6 consecutive days/mo and checked daily before 0800 hr. When captured, frogs were weighed and their snout-vent length recorded. Frogs infected with B. strigapes had the parasite removed by applying gentle pressure to the frog's skin, close to the anterior part of the larvae. This forced the larvae to exit the lymph space through the hole formed for parasite respiration. Infected animals were reweighed after parasite removal, and frogs were released at point of capture. To assess the hypothesis that Batrachomyia larvae significantly affect frog fitness, size-corrected weight data ([weight/snout-vent length] X average weight) were analyzed using ANOVA. Chi-square analyses were used to investigate other parameters. Larvae that had formed a puparium were retained to complete metamorphosis. These flies were then compared with The Australian Museum specimens to confirm parasite identification. Of 5,998 individuals from 5 frog species captured (Crinia signifera, Limnodynastes dumerilii, Limnodynastes peronii, Limnodynastes tasmaniensis, Uperoleia laevigata), only U. laevigata was parasitized with B. strigapes. Of the 1,482 U. laevigata captured, 5.1% were infected, 61 with 1 parasite, 14 with 2 parasites, and all other frogs were unparasitized. Frogs caught in warmer months (i.e., September to March) were most likely to be infected (Fig. 1), and B. strigapes abundance was positively correlated with U. laevigata abundance (r2 = 0.6145). Larvae were only observed under a parotoid gland but the level of parasitism of infected animals differed significantly between the sexes = (P1.0.05 0.0100, males 65.3%, females 34.7%). Parasites were encountered under the left parotoid (53.3%) significantly more frequently than the right (PI,0.05 = 0.0150). Fewer animals carried parasites under both parotoids (18.7%). Uperoleia laevigata infected with B. strigapes weighed significantly less (corrected for size), compared with those that were uninfected (Pj,0.0(= 0.000001). The average live weight of larvae was 0.036 g (SE 0.109) and accounted for approximately 2.5% of U. laevigata body _ weight. Larvae left their host between October and November; in the laboratory, they emerged from their puparium after approximately 28 days at 23 C (n = 8). When compared to other Australian anuran endoparasites, such as

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THE JOURNAL OF PARASITOLOGY,VOL. 87, NO. 5, October 2001

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fitness caused by the parasite burden. Alternatively, low levels of transmission may have resulted in reduced parasite burden per host. The observed low level of parasitism would be unlikely to have a major effect on the population. However, continued anthropogenic manipulation of the environment, such as habitat modification and changing climatic conditions (e.g., the green house effect, increasing levels of UV radiation) may prove detrimental to parasite-host relationships. Because empirical data on frog parasitism and its consequences are limited, there is a need for further studies to determine the contribution that these parasite-host interactions have on anuran population dynamics.

100

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0 Jan

Feb

Mar

Apr

May Jun

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Month FIGURE1. Total captures of Uperoleia laevigata and incidence of infection with Batrachomyia strigapes collected between January 1999 and April 2000 from a natural wetland in Western Sydney.

helminths (55%; Barton and Richards, 1996), the number of individuals infected was relatively low (Esch et al., 1990). Batrachomyia strigapes prevalence (5.1%) was also much lower for U. laevigata than reported for other species within the genus (i.e., 46% in C. signifera and 20% of P. bibronii; McAlpine, 1955). However, these data were obtained from frogs in the spirit collection of The Australian Museum; therefore, the samples may not accurately reflect wild population infection. Even with such potential bias, prevalence in U. laevigata is probably relatively low in the wild. In a similar study on wild populations of C. signifera, Lemckert (2000) observed that Batrachomyia atricornis infected 2.3% (n = 1,319) of animals and B. strigapes was only observed to parasitize 0.003% (n = 730) of U. laevigata. Although B. strigapes occurrence was correlated with U. laevigata abundance, environmental parameters (e.g., temperature, precipitation) that determine availability of optimum B. strigapes oviposition sites (Spring-Summer) would determine parasite prevalence. These months generally coincide with elevated invertebrate activity in the area (Warner, 1995). Anuran breeding systems, including U. laevigata, favor males that actively seek females (Stebbins and Cohen, 1995; Tyler, 1999). Males maximize reproductive success by arriving at breeding sites before females and staying longer. Male frogs therefore congregate at the edge of the ephemeral swamp (typical oviposition site for B. strigapes) for longer periods than females and are therefore presumably at a greater risk of parasitism than females. However, the preference for the left male parotoid is not so readily explained. It may be influenced by frog 'handedness' that may, in turn, influence the orientation of the head while resting. Larvae were only observed under the parotoid glands, which are prominent in Uperoleia spp. (Cogger, 2000). The associated glands are specialized for the production of protective toxins (Stebbins and Cohen, 1995). When positioned under these defensive structures, larvae may minimize vulnerability to predation. Alternatively, the abundance of blood vessels beneath the parotoids may provide for efficient access to nutrients. However, this preferred larval habitat appears to spatially restrict the level of parasitism to a maximum of 2 parasites/host (1 under each parotoid). No such restriction occurs temporally because B. strigapes larvae may emerge from their host at between 19 and 21 days under laboratory conditions (McAlpine, 1955), thus allowing for reinfection within a single season. There may therefore be at least 2 waves of infection annually, since infected animals were observed throughout spring and summer (September-March), with emergence of larvae between October and November. Under suboptimum environmental conditions, the larval stage may be extended and may potentially overwinter within their host. Frogs infected with B. strigapes larvae weighed significantly less than uninfected individuals, thereby impeding reproduction and survivorship (Cummins, 1986; Girish and Saidapur, 2000). Reduced male body condition may lead to inferior reproductive output due to impaired chorus attendance duration and, as a consequence, mate selection (Runkle et al., 1994; Bertram et al., 1996). It is hypothesized that the low number of individuals that carried multiple parasites was a reflection of lowered

LITERATURECITED D. P 1999. Ecology of helminth communities in tropical Australian amphibians. International Journal for Parasitology 29: 921926. , AND S. J. RICHARDS. 1996. Helminth infracommunities Litoria genimaculata (Amphibia: Anura) from Birthday Creek, an upland rainforest stream in Northern Queensland, Australia. International Journal for Parasitology 26: 1381-1385. BENSON, D., AND J. HOWELL. 1990. Taken for granted. The bushland of Sydney and it's suburbs. Kangaroo Press, Sydney, Australia, 160 p. BERGER, L., AND R. SPEAR. 1998. Chytridiomycosis: A new disease of wild and captive amphibians. ANZCARRT Newsletter 11: 1-3. AND J. HUMPHREY. 1997. Mucormycosis in a free, -, ranging green tree frog from Australia. Journal of Wildlife Diseases 33: 903-907. BERTRAM, S., M. BERRILL, AND E. NOL. 1996. Male mating success and variation in chorus attendance within and among breeding seasons in the Grey treefrog (Hyla versicolor). Copeia 1996:729-734. COGGER, H. G. 2000. Reptiles and amphibians of Australia. Reed New Holland, Sydney, Australia, 808 p. CUMMINS, C. P 1986. Temporary and spatial variation in egg size and fecundity in Rana temporaria. Journal of Animal Ecology 55: 303316. ESCH, G. W., A. O. BUSH, AND J. M. AHO. 1990. Parasite communities: Patterns and processes. Chapman and Hall, New York, New York, 335 p. GIRISH, S., AND S. K. SAIDAPUR. 2000. Interrelationship between food availability, fat body, and ovarian cycles in the frog, Rana tigrina, with a discussion on the role of fat body in anuran reproduction. Journal of Experimental Zoology 286: 487-493. HERO, J. M., AND G. R. GILLESPIE. 1997. Epidemic disease and amphibian declines in Australia. Conservation Biology 11: 10231025. HEYER, W. R., M. A. DONNELLY, R. W. MCDIARMID, L. C. HAYEK, AND M. S. FOSTER. 1994. Measuring and monitoring biological diversity: Standard methods for amphibians. Smithsonian Institute Press, Washington, D.C., 364 p. K. R. MCDONALD, AND R. SPEARE. 1996. Epidemic LAURANCE, W. F., disease and the catastrophic declines of Australian rainforest frogs. Biological Conservation 10: 406-413. LEMCKERT,E 2000. Parasitism of the common eastern froglet Crinia signifera by flies of the genus Batrachomyia (Diptera: Chloropidae): Parasitism rates and the influence on frog condition. Australian Zoologist 31: 492-495. MALLOCH, J. R. 1927. Notes on Australian Diptera. Proceedings of the Linnean Society of New South Wales 52: 399-441. MCALPINE,D. K. 1955. The Genus Batrachomyia (Diptera, Chloropidae). Honours thesis, Sydney University, Sydney. Australia, 15 p.

BARTON,

RUNKLE,

L. S., D. D. WELLS,

C.

C. ROBB, AND S. L. LANCE.

1994.

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