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Reproduction and Development in Halocaridina Rubra Holthuis, 1963 (Crustacea: Atyidae) Clarifies Larval Ecology in the Hawaiian Anchialine Ecosystem

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Reproduction and Development in Halocaridina Rubra Holthuis, 1963 (Crustacea: Atyidae) Clarifies Larval Ecology in the Hawaiian Anchialine Ecosystem Reference: Biol. Bull. 229: 134–142. (October 2015) © 2015 Marine Biological Laboratory Reproduction and Development in Halocaridina rubra Holthuis, 1963 (Crustacea: Atyidae) Clarifies Larval Ecology in the Hawaiian Anchialine Ecosystem JUSTIN C. HAVIRD*,†, REBECCA C. VAUGHT, DAVID A. WEESE‡, AND SCOTT R. SANTOS Department of Biological Sciences and Molette Laboratory for Climate Change and Environmental Studies, Auburn University, 101 Rouse Life Sciences Bldg., Auburn, Alabama 36849 Abstract. Larvae in aquatic habitats often develop in and significantly higher in brackish and seawater (88% and environments different from those they inhabit as adults. 72%, respectively). Correlated with this finding, identifi- Shrimp in the Atyidae exemplify this trend, as larvae of able gills capable of ion transport did not develop until many species require salt or brackish water for develop- metamorphosis into juveniles. Thus, early life stages of ment, while adults are freshwater-adapted. An exception H. rubra are apparently excluded from surface waters, within the Atyidae family is the “anchialine clade,” which which are characterized by lower and fluctuating salini- are euryhaline as adults and endemic to habitats with sub- ties. Instead, these stages are restricted to the subterra- terranean fresh and marine water influences. Although the nean (where there is higher and more stable salinity) Hawaiian anchialine atyid Halocaridina rubra is a strong portion of Hawaii’s anchialine habitats due to their in- osmoregulator, its larvae have never been observed in na- ability to tolerate low salinities. Taken together, these ture. Moreover, larval development in anchialine species is data contribute to the understudied area of larval ecology poorly studied. Here, reproductive trends in laboratory col- in the anchialine ecosystem. onies over a 5-y period are presented from seven genetic lineages and one mixed population of H. rubra; larval Introduction survivorship under varying salinities is also discussed. The Larvae in aquatic systems often undergo a prolonged devel- presence and number of larvae differed significantly among opmental stage, when they are potentially exposed to a range lineages, with the mixed population being the most prolific. of environmental conditions over a period of days to months. Statistical differences in reproduction attributable to season- Furthermore, during development, they may be exported to a ality also were identified. Larval survivorship was lowest different niche or ecosystem from adults. For example, larvae (12% settlement rate) at a salinity approaching fresh water of numerous coral reef fish species are often found in man- grove and seagrass “nurseries” (Nagelkerken et al., 2000). Received 24 February 2015; accepted 26 May 2015. However, while larvae, particularly planktonic forms, may * To whom correspondence should be addressed. E-mail: Justin. travel considerable distances (Scheltema, 1986), they often have [email protected] a limited ability to circumnavigate undesirable environments † Present address: Department of Biology, Colorado State University, (Fisher et al., 2000). Therefore, larvae at these early develop- Room E106, Anatomy/Zoology Building, Fort Collins, Colorado 80523. ‡ Present address: Department of Biological and Environmental Sci- mental stages must possess physiological mechanisms to tol- ences, Georgia College and State University, Campus Box 81, Milledge- erate a wide range of conditions, or else remain confined to a ville, Georgia 31061. relatively stable environment until later in their development. Abbreviations: COI, cytochrome oxidase I; DASPMI, 4-[4-(dimethyl- Many shrimp in the Atyidae exemplify how larvae can amino)styryl]-N methylpyridinium iodide; Halocaridina rubra colonies: experience substantially different environmental conditions EP, Eric’s Pond; EWA, Ewa Beach; HILO, Hilo, Hawaii; HM, Cape Hanamanioa; KBP, Kalaeloa Unit; KONA, Kona Coast, Hawaii; OWAI, from adults of the same species. Specifically, nearly all Waianae Boat Harbor; WC, Waianapanapa Cave; MRC, mitochondrion- atyids are freshwater stream specialists, where they can rich cell; Z1–Z4, zoeal stages 1–4. occur more than 1000 km upstream of any marine influence, 134 This content downloaded from 131.204.254.086 on May 09, 2019 14:02:34 PM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). ANCHIALINE SHRIMP DEVELOPMENT 135 and at an elevation of up to 925 m (Fryer, 1977; Hunte, Islands and elsewhere can possess appreciable haloclines, in 1979a; Hobbs and Hart, 1982). Atyids as adults are for the which waters nearing the surface are closer to 0‰ and those most part intolerant of seawater (Smith and Williams, 1981; toward the bottom approach salinities of 20‰ to 36‰ von Rintelen et al., 2012), and have no known or extant (Holthuis, 1973; Maciolek, 1983; Havird et al., 2014a). marine representatives (Fryer, 1977). The family has a Given this halocline, the larvae of H. rubra may develop in well-documented freshwater ancestry, with freshwater de- the hypogeal component of the ecosystem because it has posits of atyids dating to the Cretaceous period (Glaessner, higher and more constant salinities. To test this hypothesis, we 1969; Smith and Williams, 1981). Despite being freshwater- assessed survivorship of H. rubra larvae under laboratory adapted, many species exhibit an amphidromous life-history conditions mimicking the vertical (i.e., depth) range of salini- strategy, where larvae require brackish or salt water for ties naturally encountered in the Hawaiian anchialine ecosys- development before returning to fresh water as juveniles tem. We supplemented this assessment with a description of (Hunte, 1979a, b). This strategy can result in the export of gill development across larval stages of the species. larvae hundreds of km downstream to marine environments like estuaries, with the subsequent and spectacular return of thousands of juveniles swimming or crawling upstream Materials and Methods along stream banks (Bauer, 2013). One particular group within the Atyidae, recognized as Animals, holding conditions, and 5-y monitoring of the “anchialine clade” (von Rintelen et al., 2012), represents laboratory reproduction an apparent exception to the more or less strictly freshwater existence and amphidromous life-history strategy of the Individuals (i.e., 200–250) of Halocaridina rubra were family. With adults consistently inhabiting brackish, salt, collected using hand nets from each of eight different an- and (in some cases) hypersaline waters, members of this chialine habitats in the Hawaiian Islands during June and monophyletic clade are endemic to the anchialine ecosys- July 2006, then shipped to Auburn University, AL, within tem, which is composed of coastal ponds, pools, and caves about2dofcollections. In Hawaii, H. rubra encompasses that are fed by both fresh groundwater and marine seawater (at least) eight genetically divergent lineages with highly (Holthuis, 1973; Sket, 1996). A well-studied species of this restricted geographic ranges (Santos, 2006; Craft et al., clade is Halocaridina rubra Holthuis, 1963 from the Ha- 2008). These collections represented seven of the eight waiian Islands (Bailey-Brock and Brock, 1993). Adults of lineages, with the last coming from a population (i.e., Ka- H. rubra can survive salinities ranging from fresh water laeloa Unit colony (KBP)) that is a natural mix of two (ϳ0‰) to hypersaline (56‰) (Holthuis, 1973) via osmo- lineages (South (EWA) and West Oahu (OWAI); abbrevi- regulatory mechanisms in the gills that are atypical among ations follow Craft et al., 2008; Vaught et al., 2014)). euryhaline crustaceans (Havird et al., 2014a). Interestingly, Colonies were maintained in 38-l aquaria and in darkness larvae of H. rubra do not appear to develop identifiable gills until the late developmental stages (Havird et al., 2014a), except for 12-h light/dark cycles for one week every month. raising the question of how the larvae of anchialine species Additional details on maintenance of the H. rubra colonies such as H. rubra cope with the varying salinity regimes can be found in Vaught et al. (2014). encountered in this ecosystem. Reproduction in each H. rubra colony was visually mon- The reproductive trends and larval biology of anchialine itored, and both the number of gravid females and free- species such as H. rubra have not been extensively studied. swimming lecithotrophic (i.e., yolk-bearing) larvae (up to a Notably, over 50 years of field surveys have failed to report maximum of 100 individuals) were counted during a 10-min gravid, egg-bearing females or larvae of H. rubra in the period approximately once per week across a 5-y period (Sum- epigeal (i.e., surface) waters of Hawaii’s anchialine habitats mer 2007–Summer 2012), for a total of 185 sampling dates. (Holthuis, 1963; Maciolek, 1983; Bailey-Brock and Brock, Adult females of H. rubra (ϳ12 mm long) carry about 14–18 1993). This implies that the species undergoes reproduction large (1 mm) eggs on their abdomens for approximately 27 d, and development in the hypogeal, i.e., underground, portion then release larvae over 1 to 5 d (Iwai, 2005). Larvae develop of the ecosystem (Maciolek, 1983; Craft et al., 2008). In in the water column for about 29 d, progressing through four contrast to field surveys, laboratory studies have docu- zoeal stages and one mysis stage before metamorphosis and mented the presence of gravid females and development of settlement (Couret and Wong,
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    Anchialine restoration in Hawai‘i – One pool complex at a time Megan Lamson, Stacey Breining & Bill Gilmartin Hawai‘i Wildlife Fund (wildhawaii.org) 4th Int’l Symposium for Anchialine Ecosystems – Oct 2018 ‘Ula ka loko kāheka i ka ‘ula o loko. Sacred is the red pond where the red shrimp dwell within. B. Seidel Hawai‘i Wildlife Fund Our mission is to protect the native wildlife of Hawai‘i through research, education & conservation projects. Anchialine Pools in Hawai‘i J. Bagshaw / DOFAW B. Seidel Ka‘u Calendar Where in the …. ? C. Yuen / County of Hawai‘i Maps from: http://www.hawaiiecoregionplan.info/anchpoolNC.html Wai‘ōhinu Forest Reserve (Hawai‘i Island) 1,331 acres (538 ha) / 2 mi (3.3 km) of coastline: • Plants: 36 species of native coastal vegetation, including endangered ‘ōhai (Sesbania tomentosa) • Pools: At least 6 anchialine pools with 3 species of shrimp (Halocaridina rubra, Metabetaeus lohena, Palaemon debilis) & a cave • Petroglyphs: Several petroglyph fields & numerous other cultural resources / archeological features 1 3 2 Native wildlife utilizing pools Utah DNR Utah G. Smith / FWS M. Kimura B. Harry / NPS Native plants in/around pools Threats to anchialine ecosystems SOURBUSH CHRISTMAS BERRY SEASHORE PASPALUM LANTANA WHITE LEADTREE Misc. photographers – thank you google. Restoration Phase I (Plants) Restoration Phase II (Sediment) Restoration Phase III (Fish) Photo by John Hoover. According to Leo Nico of USGS, they ran similar bioassays in June 2018 with CFT Legumine (rotenone product) on 3 native neritid snails (Neripteron vespertinum, Neripteron vespertinum, Nerita picea) and 2 more invasive fish species: Mollies (Poecilia sphenops complex), Western Mosquitofish (Gambusia affinis) – all of which are found in anchialine pool ecosystems.
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