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Population Structure, Habitat Use, and Diet of Giant Waterbugs in a Sulfidic Cave Author(S): Michael Tobler, Katherine Roach, Kirk O

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Population Structure, Habitat Use, and Diet of Giant Waterbugs in a Sulfidic Cave Author(S): Michael Tobler, Katherine Roach, Kirk O Population Structure, Habitat Use, and Diet of Giant Waterbugs in a Sulfidic Cave Author(s): Michael Tobler, Katherine Roach, Kirk O. Winemiller, Reid L. Morehouse, and Martin Plath Source: The Southwestern Naturalist, 58(4):420-426. 2013. Published By: Southwestern Association of Naturalists DOI: http://dx.doi.org/10.1894/0038-4909-58.4.420 URL: http://www.bioone.org/doi/full/10.1894/0038-4909-58.4.420 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. THE SOUTHWESTERN NATURALIST 58(4): 420–426 DECEMBER 2013 POPULATION STRUCTURE, HABITAT USE, AND DIET OF GIANT WATERBUGS IN A SULFIDIC CAVE MICHAEL TOBLER,* KATHERINE ROACH,KIRK O. WINEMILLER,REID L. MOREHOUSE, AND MARTIN PLATH Department of Zoology, Oklahoma State University, 501 Life Sciences West, Stillwater, OK 74078 (MT, RLD) Department of Wildlife and Fisheries Sciences, Texas A&M University, 2258 TAMU, College Station, TX 77843 (KR, KOW) Department of Ecology & Evolution, University of Frankfurt, Max-von-Laue-Strasse 13, D-60438 Frankfurt am Main, Germany (MP) *Correspondent: [email protected] ABSTRACT—In the southern Mexican Cueva del Azufre, a cave ecosystem with high concentrations of toxic hydrogen sulfide, one species of hemipteran (Belostoma cf. bakeri) has adopted a unique ecological function in that it acts as one of the top predators in the subterranean food web, preying on the abundant cavefish Poecilia mexicana. To date, several aspects of this predator-prey interaction have been explored, but basic questions related to the ecology of the waterbugs remained unstudied. We tested whether there is evidence for reproduction of waterbugs within the cave, which would indicate a self-sustaining population. Furthermore, we investigated the habitat affinities of different size-classes of waterbugs. We infer that waterbugs reproduce inside the cave despite the toxic properties of the water, as evidenced by the presence of nymphs of all sizes and males carrying developing zygotes. We also found size-dependent differences in use of habitat, and particularly small nymphs occupy different microhabitats than larger individuals. Adult waterbugs and large nymphs were most common at sites with cavefish. Small nymphs were rare at these locations, possibly to avoid cannibalism or exploit different resources in other locations. Furthermore, stable-isotope-analysis indicated that waterbugs likely derive their carbon from a combination of fish, dipteran larvae, and chemoautotropic bacteria. RESUMEN—En el sur de M´exico en la Cueva del Azufre, un ecosistema cavern´ıcola con altas concentraciones del t´oxico sulfuro de hidr´ogeno, una especie hem´ıptera (Belostoma cf. bakeri) ha adoptado una funci´on ecol´ogica unica,´ actua´ como uno de los depredadores m´as altos de la red alimentaria subterr´anea, comiendo el abundante pez de la cueva, Poecilia mexicana. Hasta la fecha, varios aspectos de esta interacci´on entre el depredador y su presa han sido estudiados, pero preguntas b´asicas relacionadas a la ecolog´ıa de B. bakeri se mantienen sin estudio. Examinamos si se encuentra evidencia de reproducci´on en B. bakeri adentro de la cueva, lo que indicar´ıa que la poblaci´on es autosostenible. Tambi´en investigamos las afinidades del h´abitat de diferentes clases de tamano˜ de B. bakeri. Dedujimos que B. bakeri se reproduce adentro de la cueva a pesar de las propiedades t´oxicas del agua, en base a la presencia de ninfas de todos tamanos˜ y de los machos cargando cigotos en desarrollo. Tambi´en encontramos diferencias en uso de h´abitat segun´ el tamano˜ corporal, especialmente que las ninfas pequenas˜ ocupan microh´abitats diferentes que individuos m´as grandes. Adultos y ninfas grandes fueron m´as comunes en sitios con peces de la cueva. Las ninfas pequenas˜ casi no se encontraron en estos sitios, posiblemente para evitar el canibalismo o para explotar otro tipo de recursos en otros lugares. Adem´as, el an´alisis de is´otopos estables indic´o que B. bakeri probablemente deriva su fuente de carb´on al ingerir peces, larva de d´ıpteros, y bacterias quimioautotr´oficas. Giant waterbugs of the family Belostomatidae are large Jordan, 1996; Mori and Ohba, 2004; Ohba and Nakasuji, aquatic hemipterans with extra-oral digestion that prey on 2006; Swart et al., 2006), the smaller-bodied species of the a variety of invertebrates and vertebrates (Menke, 1979). subfamily Belostomatinae prey on various terrestrial and They are sit-and-wait predators that catch bypassing prey aquatic invertebrates and anurans but usually avoid fish with their strongly incrassate, raptorial forelegs. Upon (Cullen, 1969; Swart and Felgenhauer, 2003; Ohba and capture, belostomatids inject toxins causing paralysis of Nakasuji, 2006; Swart et al., 2006). prey and digestive enzymes causing necrosis of tissue Among the most unusual environments inhabited by (Swart and Felgenhauer, 2003; Swart et al., 2006). While giant waterbugs is a Mexican sulfur cave, the Cueva del the large-bodied species of the subfamily Lethocerinae Azufre (Gordon and Rosen, 1962). The stream within this have been widely reported to feed on large prey including cave is fed by a number of springs containing toxic small snakes, anurans, and most notably fish (Babbitt and hydrogen sulfide (Tobler et al., 2006). Despite the toxic December 2013 Tobler et al.—Ecology of giant waterbugs 421 FIG. 1—a) Belostoma are predators of cavefish. Depicted is a waterbug (28 mm) foraging on a cavefish in situ. The white coating on the back of the abdomen and legs of the waterbug are filaments of sulfide bacteria. b) Sketch of the study area (surveyed area outlined by dashed line) depicting the major watercourses in the Cueva del Azufre. Light gray areas are dry land within the cave, dark areas indicate impenetrable bedrock, and areas in intermediate gray shading represent aquatic habitats. conditions, the cave harbors a diverse fauna of terrestrial of adult Belostoma in one of the front chambers of the and aquatic organisms (Summers Engel, 2007), including Cueva del Azufre (Tobler et al., 2007), but it is still a unique population of cavefish (cave mollies, Poecilia unclear whether the waterbugs reproduce within the cave. mexicana, Poeciliidae). These fish, similar to many other Alternatively, the cave with its high densities of fish might cave organisms (Porter and Crandall, 2003), exhibit simply be a temporary feeding habitat for adults, or a reduced eye-size and pigmentation of the body but also population sink. We consequently conducted a thorough have evolved enhanced nonvisual senses and are able to survey to estimate the structure of the population of communicate in darkness (Plath et al., 2004; Tobler et al., Belostoma within the cave and searched for signs of 2008b, 2008c). Within the Cueva del Azufre, giant water- recruitment of juvenile waterbugs inside the cave and bugs of the genus Belostoma (subfamily Belostomatidae) for males carrying eggs. In the subfamily Belostomatinae, and cave mollies exhibit a unique predator-prey relation- males exhibit post-copulatory paternal care as females lay ship (Fig. 1a). Due to the toxic effects of hydrogen sulfide their eggs directly on the back of males, and males carry and the extreme hypoxia in the water, cave mollies spend the eggs until developed offspring hatch (Lauck and long periods of time performing aquatic surface respira- Menke, 1961; Kruse, 1990; Gilg and Kruse, 2003). Hence, tion (skimming the micro-layer of water at the surface reproduction in waterbugs is relatively easy to detect. In with relatively higher concentration of dissolved oxygen addition, we analyzed use of microhabitat by the water- and passing it over the gill filaments during opercular bugs and particularly tested for ontogenetic shifts. ventilation). While performing aquatic surface respira- Because cannibalism can be intense in giant waterbugs tion, cave mollies are vulnerable to attacks by giant (Ohba et al., 2006; Swart et al., 2006), nymphs may avoid waterbugs lurking at the surface of the water (Tobler et microhabitats preferred by larger conspecifics, or juve- al., 2009). Waterbugs preferentially prey upon large- niles may exploit different resources underrepresented in the microhabitats with larger waterbugs. Finally, even bodied individuals over small ones (Plath et al., 2003; though Belostoma readily feed on cavefish in an experi- Tobler et al., 2007), gestating over nongestating females mental setting and can occasionally be observed in situ (Plath et al., 2011), and males over females (Tobler et al., capturing fish (Fig. 1a), it is unclear to what extent the 2008a). Consequently, waterbugs potentially affect the giant waterbugs rely on fish as an energy source,
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