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Pitch Lake Water Protects Guppies (Poecilia Reticulata) from Microbial and Gyrodactylid Infections

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Pitch Lake Water Protects Guppies (Poecilia Reticulata) from Microbial and Gyrodactylid Infections View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by University of East Anglia digital repository 1 Parasites pitched against nature: Pitch Lake water protects guppies (Poecilia reticulata) from microbial and gyrodactylid infections BETTINA SCHELKLE1, RYAN S. MOHAMMED2,MICHAELP.COOGAN3, 4 1 4 MARK MCMULLAN , EMMA L. GILLINGHAM , COCK VAN OOSTERHOUT and JOANNE CABLE1* 1 School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK 2 Department of Life Sciences, University of the West Indies, St Augustine, Trinidad, West Indies 3 School of Chemistry, Cardiff University, Cardiff CF10 3AT, UK 4 School of Environmental Sciences, University of East Anglia, Norwich Research Park, Norwich NR4 7TJ, UK (Received 23 April 2012; revised 18 May 2012; accepted 21 May 2012) SUMMARY The enemy release hypothesis proposes that in parasite depleted habitats, populations will experience relaxed selection and become more susceptible (or less tolerant) to pathogenic infections. Here, we focus on a population of guppies (Poecilia reticulata) that are found in an extreme environment (the Pitch Lake, Trinidad) and examine whether this habitat represents a refuge from parasites. We investigated the efficacy of pitch in preventing microbial infections in Pitch Lake guppies, by exposing them to dechlorinated water, and reducing gyrodactylid infections on non-Pitch Lake guppies by transferring them to Pitch Lake water. We show that (i) natural prevalence of ectoparasites in the Pitch Lake is low compared to reference populations, (ii) Pitch Lake guppies transferred into aquarium water develop microbial infections, and (iii) experimentally infected guppies are cured of their gyrodactylid infections both by natural Pitch Lake water and by dechlorinated water containing solid pitch. These results indicate a role for Pitch Lake water in the defence of guppies from their parasites and suggest that Pitch Lake guppies might have undergone enemy release in this extreme environment. The Pitch Lake provides an ideal ecosystem for studies on immune gene evolution in the absence of parasites and long-term evolutionary implications of hydrocarbon pollution for vertebrates. Key words: antihelminthic, asphalt, Pitch Lake, Gyrodactylus, Poecilia reticulata, enemy release. INTRODUCTION et al. 2007), yet, their effects on parasites infecting hosts inhabiting such environments are rarely Host parasite co-evolution acts to maintain poly- assessed, even though they can have a major impact morphism and/or increase the rate of molecular on the host-parasite relationships. Populations of evolution (Lively, 1987; Dybdahl and Lively, 1998; guppies with little or no parasites are rare (see Fraser Lively and Jokela, 2002; Decaestecker et al. 2007; and Neff, 2010), but preliminary investigations Woolhouse et al. 2002; Paterson et al. 2010). With indicate that the Pitch Lake may be one such habitat the majority of all free-living animals hosting at least (Cable, 2011). 1 parasite taxon (Price, 1980), populations without The Pitch Lake (Fig. 1) consists of a natural parasites represent a rare opportunity to understand upwelling of oils that contain hydrocarbons, sulphur, the effects of host-parasite co-evolution. Island metals and volcanic ash at concentrations usually populations may experience reduced selection press- considered toxic to living organisms (Peckham, ures due to decreased parasite diversity, prevalence 1895; Ponnamperuna and Pering, 1967; Burgess and intensity (e.g. Lindström et al. 2004), similar to et al. 2005; World Health Organization Concise invasive species that are released from their natural International Chemical Assessment Document, enemies in novel environments (Liu and Stiling, 2005; Marković et al. 2007). It is the largest asphalt 2006). A special case of ‘enemy release’ may be lake in the world (ca. 0·8 km2), resembling a experienced by populations in extreme environments volcano crater, located on the south west coast of in which hosts may find refuge from their parasites Trinidad. Only 4 other asphalt lakes exist worldwide: (Tobler et al. 2007). The adaptive forces in these the La Brea tar pits, the McKittrick tar pits, hostile habitats are often well defined (Amils Pibernat Carpinteria tar pits (all 3 in California, USA) and Lake Guanoco (Venezuela). Although such lakes have * Corresponding author: School of Biosciences, Cardiff University, Cardiff CF10 3AX, UK. Tel: been the focus of many paleoecological studies (e.g. ++44 (0) 20 298 76022. Fax: +44 (0)29 208 74116. Coltrain et al. 2004), little is published on their E-mail: cablej@cardiff.ac.uk extant biodiversity (Kadavy et al. 1999; Ali et al. 2006; Parasitology, Page 1 of 8. © Cambridge University Press 2012 doi:10.1017/S0031182012001059 Bettina Schelkle and others 2 Fig. 1. The Pitch Lake, Trinidad. Insert: a close-up on one of the pools where guppies were collected for this study. Schulze-Makuch et al. 2010) or on the evolution of occurrence is mainly characteristic of lowland guppy species in this habitat (but see Tezuka et al. 2011). populations, whereas the Trinidadian upland popu- Despite its hostile environment, freshwater pools lations are occasionally free of gyrodactylids (Martin amongst the pitch folds of the encrusted Pitch Lake and Johnson, 2007; Fraser and Neff, 2010). The surface are a habitat for plants (e.g. Nymphaea and difference in gyrodactylid load may be explained by Nitella; personal observations), bacteria (e.g. Pseudo- the fact that upland host populations are relatively monas; see Ali et al. 2006; Schulze-Makuch et al. small in census population size and have arisen from 2010), invertebrates (e.g. dragon fly larvae, aquatic founder events, whilst being connected by a very beetles; personal observations), the amphibian Pseudis limited amount of upstream migration (Barson et al. paradoxa ( personal observations) and fish (e.g. Poecilia 2009). Furthermore, given that parasitized guppies reticulata, Rivulus hartii, see Burgess et al. 2005; and are more likely to be flushed downstream (van Polycentrus schomburgkii, personal observations). Oosterhout et al. 2007) some upland populations The guppy (Poecilia reticulata), a small, hardy appear to be parasite-free, either due to failure of freshwater fish, is found throughout Trinidad and parasite establishment or subsequent parasite popu- Tobago as well as in Venezuela, Guyana and Surinam lation extinction. Hence, the guppies in some upland (Magurran, 2005). Throughout their natural habitat, populations such as the Upper Naranjo have been guppies are parasitized by the ectoparasitic, her- shown to be devoid of gyrodactylids for almost a maphroditic gyrodactylids (for exceptions, see decade ( personal observations) and can be regarded as Martin and Johnson, 2007; Fraser and Neff, 2010). naive to these parasites. Despite being helminths, Gyrodactylus species are In the present study, we compare parasite burdens regarded as microparasites (Scott and Anderson, in the field with published data and assess the 1984) due to their multi-modal, hyperviviparous importance of the pitch environment for the health reproductive system (Cable and Harris, 2002; Bakke of guppies using experimentally infected fish. In Part et al. 2007). In natural populations of guppies, 1, parasite infections are assessed for the Pitch Lake gyrodactylids often occur at prevalences of up to guppy population. Having confirmed the absence of 75% (van Oosterhout et al. 2007). Such high parasite Gyrodactylus spp. in the Pitch Lake, we hypothesized Enemy release in an extreme environment 3 Table 1. Minimum and maximum water physico-chemistry values of the Pitch Lake and three riverine sites in Trinidad recorded in different seasons between 2003 and 2012 Pitch Lake Upper Naranjo Mid Naranjo Lower Aripo pH 2·8–8·4 7·6–9·35 7·4–7·6 7·1–8·8 Temperature °C 26·1–32·5 23·1–25·4 23·0–23·4 23·7–25·9 Salinity gL−1 0·1–0·7 0·1–0·2 0·1 0·0–0·2 Conductivity μS 404–1649 120–402·5 210–235 232–328 Dissolved oxygen mgL−1 0·7–2·32 5·42–7·8 5·15–8·99 2·1–8·77 that Pitch Lake water had significant anti-parasitic of guppies (n=10) for Experiment 1 plus 20 guppies properties. Therefore, in Part 2, we experimentally for Experiment 2 (Part 2) were collected from investigated the effect of Pitch Lake water on fungal the Upper Naranjo (UTM 20P: 692498.44 E, and/or bacterial (from hereon: microbial) and hel- 118257.53 N), a tributary of the Aripo River that minth infections in guppies. Firstly, we exposed originates in the Northern mountain range of Pitch Lake guppies to aquarium water and Trinidad and flows into the Caroni drainage. Gyrodactylus bullatarudis infected fish to Pitch Lake water. Secondly, we directly exposed G. turnbulli infected, ornamental guppies to dechlorinated Part 1: Natural parasite fauna aquarium water containing solid pitch or to artifi- For the parasite analysis of Pitch Lake guppies, cially produced pitch water of varying ages. By samples from 2004, 2006 and 2007 were analysed for producing pitch water of varying ages, we also tested gyrodactylid prevalence, mean intensity and range. whether the antihelminthic compounds are chemi- The preserved fish were transferred to a Petri dish cally unstable or volatile to provide an overview of the and completely immersed in ethanol. Using a anti-parasitic properties of Pitch Lake water. dissecting microscope the surface of the fish was scanned and any parasites recorded. The ethanol in which the fish had been originally fixed was also MATERIALS AND METHODS screened for any dislodged parasites. Gyrodactylid This study was approved by the Cardiff University parasites were removed from their host using insect Animal Ethics Committee and regulated by a UK pins and transferred onto a microscope slide. Home Office licence (PPL 30/2357). Specimens were mounted in ammonium picrate glycerine after partial digestion (Harris et al. 1999) and examined for differences in haptor morphology Sampling sites to identify worms to species level. Guppies (SL: 9·1–22·4 mm) were collected from the Pitch Lake (grid reference UTM 20P: 650341.45 E, Part 2: Experimental transfer 1131668.93 N; Fig.
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