Preliminary Evaluation of the Potential of the Helminth Parasite Rhabdias
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Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy Biological Control 54 (2010) 69–74 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Preliminary evaluation of the potential of the helminth parasite Rhabdias elegans as a biological control agent for invasive Puerto Rican coquís (Eleutherodactylus coqui) in Hawaii Shenandoah R. Marr a, Steve A. Johnson b,c,*, Arnold H. Hara a, Monica E. McGarrity c a Beaumont Agricultural Research Center, College of Tropical Agriculture and Human Resources, University of Hawaii at Ma¯noa, 875 Komohana Street, Hilo, HI 96720-4037, USA b Department of Wildlife Ecology, University of Florida Institute of Food and Agricultural Sciences, 110 Newins-Ziegler Hall, P.O. Box 110430, Gainesville, FL 32611-0430, USA c Gulf Coast Research and Education Center, University of Florida Institute of Food and Agricultural Sciences, 1200 North Park Road, Plant City, FL 33563-1540, USA article info abstract Article history: In Hawaii, the extremely loud mating calls of invasive Puerto Rican coquís (Eleutherodactylus coqui Tho- Received 11 August 2009 mas) depress real estate values in infested areas and reduce tourist appeal, with significant economic Accepted 25 April 2010 repercussions. Measures required to prevent inter-island transport of frogs also result in substantial costs Available online 29 April 2010 for the floriculture industry. Classical biological control has been used successfully for over 100 years to combat invasive insects in Hawaii, and there is considerable interest in developing similar controls for Keywords: coquís. Since Hawaii lacks native amphibian and reptile faunas (with the exception of marine species), Eleutherodactylus coqui the risk of unintended effects of a biological control agent on non-target species would be minimal. Rhabdias elegans We identified Rhabdias elegans Gutierrez, a helminth parasite of native Puerto Rican populations of Anuran Invasive E. coqui that is not found in introduced Hawaiian populations, as a prime candidate for investigation Biological control as a potential biological control. We conducted laboratory experiments to evaluate overt effects of Lung nematode R. elegans on growth, survival, and locomotory performance of E. coqui from Hawaii. Experimental Growth infection with R. elegans did not directly affect growth, survival, or endurance of E. coqui maintained under Survival optimal laboratory conditions, but significantly reduced initial locomotory burst performance. We suggest Locomotory performance that R. elegans holds limited potential as a biological control agent for eradication of E. coqui, but warrants additional investigation under more natural conditions of its potential for use as a management tool. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction ever, macroparasite effects on amphibian populations may be sig- nificant (Anderson, 1980), and analysis of these effects could Parasites often exert a negative influence on the behavior, provide valuable information for efforts to conserve imperiled spe- growth, size, fecundity, and even survival of the host (reviewed cies and manage invasive species. by Minchella and Scott, 1991). Recently, such effects of parasites Nematode macroparasites of the genus Rhabdias (Nematoda: on amphibian hosts have received an increasing amount of atten- Rhabdiasidae) commonly infect amphibians and reptiles through- tion (e.g., Tinsley et al., 2002; Johnson et al., 2006, 2008; Dare out the world, living in association with a specific host (Anderson, and Forbes, 2008; Koprivnikar et al., 2008). However, there is a 2000). Parasitic adults live as protandrous hermaphrodites (acting paucity of experimental data on the majority of naturally occurring as functional males before becoming functional females) in the host–parasite relationships, particularly for those involving lungs of the host, where they deposit eggs that then pass up the amphibian hosts. Many studies of amphibian parasites are descrip- respiratory tract to the oral cavity and are swallowed. The eggs tive and focus on parasite life cycles and taxonomy (e.g., Kuzmin hatch in the intestine, releasing first-stage larvae that accumulate et al., 2003, 2007; Dubey and Shine, 2008; Langford and Janovy, in the colon and are voided in the feces. Free-living first-stage lar- 2009) or host susceptibility (e.g., Dare and Forbes, 2009a,b) rather vae undergo a series of molts in the external environment, eventu- than on pathogenic effects on the host. Studies of pathogens ally developing into infective third-stage larvae. These infective thought to contribute to global amphibian decline (reviewed by larvae penetrate the skin of a host and migrate into the body cavity Daszak et al., 2003) are among the only studies to evaluate effects where they grow into late third and fourth stages, and finally into of amphibian parasites, but largely ignore macroparasites. How- parasitic subadults. Subadults must then invade the lungs in order to mature and produce eggs (Baker, 1979). Investigations of the effects of nematodes of the genus Rhabdias * Corresponding author at: University of Florida/IFAS – GCREC, 1200 North Park suggest that this naturally-occurring parasite may have significant Road, Plant City, FL 33563-1540, USA. E-mail address: tadpole@ufl.edu (S.A. Johnson). negative effects on some amphibian species (Goater, 1992, 1994; 1049-9644/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2010.04.012 Author's personal copy 70 S.R. Marr et al. / Biological Control 54 (2010) 69–74 Goater and Ward, 1992; Goater et al., 1993; Goater and Vandenbos, Most importantly, the risks of impacts to non-target species and 1997; Kelehear et al., 2009). Experimental infection of juvenile spread of the control agent to unintended areas must be minimal common toads (Bufo bufo L.) with varying doses of infective stage (Simberloff and Stiling, 1996; Hoddle, 2004; Messing and Wright, Rhabdias bufonis Schrank (Nematoda: Rhabdiasidae) larvae re- 2006). With the exception of marine species, all of Hawaii’s herpe- sulted in a decrease in toad growth, food intake, and survival, sug- tofaunal species are introduced (P11 species established), thus gesting that R. bufonis infection could adversely affect host concerns regarding host specificity are minimal. Spread or dis- population size (Goater and Ward, 1992). Experimental infection persal of biological control agents is also a concern, but measures with R. bufonis also reduced endurance of juvenile B. bufo; time currently used to prevent the spread of E. coqui should also prevent and distance traveled by toads before exhaustion decreased signif- transport and introduction of infected frogs and their associated icantly in both low and high parasite exposure groups (Goater parasites in sufficient numbers to maintain the parasite life cycle. et al., 1993). Similarly, experimental infection of cane toads (Rhi- Therefore, the potential benefits of using biological control agents nella [formerly Bufo] marina L.) with Rhabdias cf. hylae Barton to manage E. coqui in Hawaii warrant identification and evaluation (Nematoda: Rhabdiasidae) significantly reduced toad growth, sur- of potential agents. When biological control is deemed a viable op- vival, and locomotory performance (Kelehear et al., 2009). Heavy tion for management of an invasive species, candidate biological infections of Rhabdias spp. in captive amphibians have been found control agents are selected from the natural predators, parasites, to cause pulmonary damage, predispose amphibians to secondary or pathogens of the invasive species, and should exert the maxi- infections, and even cause death (Williams, 1960; Poynton and mum impact on the target species (Simberloff and Stiling, 1996; Whitaker, 2001). Analysis of the effects of parasite infection on Hoddle, 2004; Messing and Wright, 2006). In the case of E. coqui non-native amphibians could provide valuable information for ef- in Hawaii, helminth parasites of the genus Rhabdias are a prime forts to manage populations that are increasing rapidly and nega- candidate for evaluation as a potential biological control. tively impacting local ecosystems and/or economies, as is the In their native range in Puerto Rico, E. coqui have a diverse par- case with Puerto Rican coquís in Hawaii. asite fauna dominated by helminths (Dyer et al., 1995; Marr et al., The Puerto Rican coquí, Eleutherodactylus coqui Thomas (Anura: 2008), with Rhabdias elegans Gutierrez detected at prevalences of Leptodactylidae), was accidentally introduced to the Hawaiian Is- >25% (Burrowes et al., 2004; Marr et al., 2008). However, parasite lands prior to 1988 via the ornamental plant trade, and populations surveys of E. coqui in Hawaii have failed to detect R. elegans (Gold- rapidly expanded (Kraus and Campbell, 2002).