Original articleExtreme habitats as refuge from parasite infections? Evidence from an extremophile fish
Introduction
Living under extreme environmental conditions is usually associated with costs; however, very little is known about potential benefits. Townsend et al. (2003) point this out by defining an extreme environmental condition as one that requires, of any organism tolerating it, costly adaptations absent in most related species. These can include changes in morphology and physiological pathways that allow coping with a physiochemical stressor, as well as behavioral adaptations and shifts in life history strategies. But why do organisms colonize extreme habitats if there are immediate costs ranging from the investment towards specific adaptations to an increased risk of death?
Given the associated costs, it could be argued that the organisms become trapped in an extreme habitat. However, many extreme habitats are not isolated but contiguous, and no permanent discontinuity prevents organisms from returning to their original habitat. Colonizing extreme habitats would be directly advantageous when individuals that have the ability to cope with the extreme environment confer an advantage compared to relatives living in non-extreme habitats. Selection favoring individuals with adaptations will lead to adaptive shifts within populations as colonizers of extreme habitats exploit new and unused niches (Romero and Green, 2005).
In either way, if organisms persist in extreme habitats over evolutionary time scales, resource investment into the costly adaptations that allow for survival must be traded off. Thus, organisms living in extreme habitats have to invest more into specific adaptations, but they also may maintain or even increase their fitness compared to adjacent populations in non-extreme habitats. Since extreme habitats often harbor impoverished biocoenoses (Begon et al., 1996), the advantages of living in extreme habitats may include the reduction of competition and predation and the exploitation of new niches (Romero and Green, 2005); however, very few tests of these ideas have thus far been published.
Another potential advantage of living in an extreme habitat that has received no attention so far is that such habitats may act as “refuge” from parasites and diseases. Parasites are ubiquitous, and infections often have significant consequences for the host. Parasites can directly affect viability and fertility of the host with consequences for the host's reproductive fitness (Bush et al., 2001). By avoiding or at least reducing the infection risk by parasites, hosts may increase their fitness and thereby trade off costly adaptations needed to survive in an extreme habitat.
There are basically two proximate mechanisms that can lead to a decreased risk of a parasite infection in extreme habitats (Fig. 1). Firstly, physiochemical stressors can have the same direct detrimental effect on free-living parasite stages as on every other organism. Thus, unless the parasite has the same ability to cope with the extreme environment as the host, it will be less successful and may even disappear from the habitat. Secondly, many parasites have indirect life cycles and rely on more than one host species as they go through different developmental stages. The lack of any necessary host species that does not survive in the extreme habitat interrupts the life cycle of the parasite. Thus, the absence of an obligate host species indirectly leads to the local extinction of the parasite.
Based on this hypothesis, two empirically testable hypotheses can be made. (1) Given that a parasite species has at least one of the above mentioned characters (free-living stages or multiple host species), its prevalence should be reduced in more extreme habitats. (2) On the level of parasite communities, it is predicted that hosts in more extreme habitats harbor fewer parasite species. Furthermore, parasite communities should generally shift towards species with a direct life cycle, species lacking long lasting free-living stages and species living inside rather than on their hosts.
A potential model system to test this hypothesis is a small livebearing fish, the Atlantic molly (Poecilia mexicana Steindachner, Poeciliidae), which is widely distributed on the Atlantic versant from northern Mexico to northern Costa Rica (Miller, 2005). Besides normal stream and river habitats, this species also inhabits a limestone cave (the Cueva del Azufre) drained by a creek (Gordon and Rosen, 1962). The cave population of P. mexicana is also known as the Cave molly (Parzefall, 2001). The creek running through the Cueva del Azufre is fed by several springs with high concentrations of hydrogen sulfide (H2S, Tobler et al., 2006). It eventually leaves the cave and forms a sulfurous surface creek, El Azufre.
Hydrogen sulfide is highly toxic for all animals, because it binds to the iron of the heme to replace O2. It also binds at the cytochrome c oxidase, where it prohibits electron transport in aerobic respiration (Lovatt Evans, 1967, Stallones et al., 1979, Grieshaber and Völkel, 1998). In the cave, H2S ranges from 10 to 300 μM; such concentrations usually are considered toxic (Arp et al., 1992, Völkel and Grieshaber, 1992). Consequently, the Cueva del Azufre and El Azufre can be viewed as extreme habitats (Tobler et al., 2006). How P. mexicana copes with H2S is so far not well understood. A costly behavioral adaptation, aquatic surface respiration (ASR), where fish exploit the air–water interface, has been shown to be crucial for the survival in sulfidic water (Plath et al., submitted). Other fish are able to detoxify sulfide to some extent, e.g. by oxidizing sulfide to thio-sulfate (Bagarinao and Vetter, 1990), but physiological adaptations to H2S remain to be studied in P. mexicana.
It has been suggested that in the Cueva del Azufre chemoautotrophic primary production provides ad libitum amounts of food for the mollies (Langecker et al., 1996). Mollies from sulfurous habitats, however, are in a worse nutritional state than mollies from non-extreme habitats and have a lower body condition, indicating that energy may in fact be limited (Plath et al., 2005, Tobler et al., 2006). Compared to adjacent surface habitats, the Cueva del Azufre and El Azufre harbor an impoverished fish fauna with P. mexicana as the predominant species (Tobler et al., 2006). Hence, interspecific competition for resources and predation by piscivorous fishes is reduced in the sulfidic habitats.
Other potential benefits of colonizing the Cueva del Azufre might also play a role in this system. Thus, we asked if living in an extreme habitat confers an advantage to P. mexicana with regard to a reduced risk of parasite infection by testing the first of the aforementioned predictions. Mollies are known to harbor a diverse parasite fauna (Tobler and Schlupp, 2005, Tobler et al., 2005; Tobler, unpublished data). One of the most prevalent species is the digenean trematode Uvulifer sp., the metacercariae of which provoke the production of a fibrous capsule of host tissue around the parasite, which is followed by the migration of melanocytes into the cyst's wall, creating the characteristic appearance of a black spot (black spot disease, BSD; Spellman and Johnson, 1987, Bush et al., 2001). This reaction of the host is assumed to be costly, since the penetration of the skin causes mechanical damage. Until the parasite becomes encapsulated, the host's metabolic demand increases significantly so that energy reserves may decline. Uvulifer sp. has an indirect life cycle (Fig. 1). After encapsulation in the fish host, the parasite remains dormant until the intermediate host is consumed by a piscivorous bird, the final host in which the parasite reproduces sexually. Water snails are the first intermediate hosts in which the parasite multiplies asexually, and free-swimming cercariae are produced. These cercariae infect fishes as second intermediate hosts by penetrating the skin and transform into encysted metacercariae. This parasite thus has both characters to test the first prediction formulated above.
In the present study, we compared parasitization of P. mexicana by Uvulifer sp. among different extreme and non-extreme habitats. Furthermore, we attempted to investigate whether a potential reduction of parasitism in extreme habitats is caused by selection on free-living parasite stages or on other host species.
Section snippets
Field sites
All study sites are located near the village Tapijulapa in Tabasco, Mexico. The creeks studied eventually drain into the Río Oxolotan. The Río Oxolotan itself joins the Río Amatán and forms the Río Tacotalpa, a tributary of the Río Grijalva-system.
We caught P. mexicana in cave chambers III, IV, V, X and XIII of the Cueva del Azufre (Gordon and Rosen, 1962). Additionally, fish were caught in El Azufre, a surface habitat containing toxic H2S. Currently, these are the only known sulfidic waters
Parasite prevalence and intensity
The prevalence of BSD differed significantly between populations, whereby Uvulifer sp. was most prevalent in Arroyo Cristal, less prevalent in El Azufre and absent in the cave (Table 1, χ2 = 218.69, P < 0.001; α′ = 0.0125). The significant difference between populations was not only driven by eminently low prevalence of Uvulifer sp. within the cave, because when the prevalence was only compared between El Azufre and Arroyo Cristal, the difference was still significant (χ2 = 21.017, P < 0.001; α′ = 0.0125).
Discussion
Parasitism in Poecilia mexicana through Uvulifer sp. was high in the non-extreme surface habitat and reduced in habitats containing hydrogen sulfide. Within the cave, fish infected with BSD were absent from our samples. H2S concentrations are especially high within the cave (Tobler et al., 2006) and potential final and intermediate hosts of Uvulifer sp. were absent. In contrast, potential final and intermediate hosts were present in both surface habitats, but snails were less abundant in the
Acknowledgments
We are grateful to the people of Tapijulapa for their hospitality during our visits. C. Dames prepared the snails. N. Tobler prepared Fig. 1. C. Franssen and four anonymous reviewers helped to improve an earlier version of the manuscript. The Mexican government kindly issued permits (Permiso de pesca de fomento numbers: 291002-613-1577 and DGOPA/5864/260704/-2408) to conduct this research. Financial support came from the DFG (SCHL 344/15-1; PL 470/1-1) as well as the Basler Foundation for
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2020, Acta OecologicaCitation Excerpt :The Pathogen Refuge Hypothesis posits that one potential side-benefit of invading extreme environments might come into play if these environments act as a refuge from parasites and other pathogens, which could partially balance out the costs associated with survival (at an early stage) and local adaptation (at a later stage) to the extreme conditions (Kruckeberg, 1992; Springer et al., 2007; Tobler et al., 2007a). While recent research has shown that extreme environments are not entirely free of parasites (Tinsley, 1999; Martinez and Merino, 2011; Carlsson et al., 2012; Tobler et al., 2014), several studies have indeed provided evidence for a reduction of at least certain types of parasites in extreme habitats (e.g., oil-pollution and ectoparasites on guppies, Poecilia reticulata: Schelkle et al., 2012; pathogens on serpentine flax, Hesperolinon spp.: Springer, 2009; fish ectoparasites in toxic hydrogen sulphide-rich habitats: Tobler et al., 2007a; high salinity and chytrid fungus infections in eastern dwarf tree frogs, Litoria fallax: Stockwell et al., 2015; but see Springer et al., 2007). Here, we make use of the well-established study system of Mexican livebearing fishes (family Poeciliidae) undergoing population divergence and speciation in toxic hydrogen sulphide (H2S)-rich aquatic habitats (Tobler et al., 2018).