View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by College of William & Mary: W&M Publish W&M ScholarWorks VIMS Articles 2016 Effects of Embryonic Exposure to Salinity Stress or Hypoxia on Post-metamorphic Growth and Survival of the Polychaete Capitella teleta JA Pechenik OR Chaparro A Pilnick M Karp Virginia Institute of Marine Science M Acquafredda See next page for additional authors Follow this and additional works at: https://scholarworks.wm.edu/vimsarticles Part of the Zoology Commons Recommended Citation Pechenik, JA; Chaparro, OR; Pilnick, A; Karp, M; Acquafredda, M; and Burns, R, "Effects of Embryonic Exposure to Salinity Stress or Hypoxia on Post-metamorphic Growth and Survival of the Polychaete Capitella teleta" (2016). VIMS Articles. 1690. https://scholarworks.wm.edu/vimsarticles/1690 This Article is brought to you for free and open access by W&M ScholarWorks. It has been accepted for inclusion in VIMS Articles by an authorized administrator of W&M ScholarWorks. For more information, please contact [email protected]. Authors JA Pechenik, OR Chaparro, A Pilnick, M Karp, M Acquafredda, and R Burns This article is available at W&M ScholarWorks: https://scholarworks.wm.edu/vimsarticles/1690 Reference: Biol. Bull. 231: 103–112. (October 2016) © 2016 Marine Biological Laboratory Effects of Embryonic Exposure to Salinity Stress or Hypoxia on Post-metamorphic Growth and Survival of the Polychaete Capitella teleta JAN A. PECHENIK1,*, OSCAR R. CHAPARRO2, AARON PILNICK1, MELISSA KARP1,†, MICHAEL ACQUAFREDDA1,‡, AND ROBERT BURNS1 1 Department of Biology, Tufts University, Medford, Massachusetts 02155; and 2 Instituto de Ciencias Marinas y Limnolo´gicas, Universidad Austral de Chile, Valdivia, Chile Abstract. Although a good number of studies have Introduction investigated the impact of larval experience on aspects of post-metamorphic performance, only a few have consid- Latent effects occur when a stress that is experienced ered the potential impact of stresses experienced by during early development manifests itself following meta- brooded embryos. In this study we separately investi- morphosis (Pechenik, 2006). These effects have been doc- gated the impact of salinity stress (as low as 10) and umented in response to a variety of environmental stressors Ϫ1 such as exposure to sublethal pollutant concentrations (e.g., hypoxia (1 ml O2 l ) experienced by brooded embryos of the deposit-feeding polychaete Capitella teleta on Ng and Keough, 2003; Nice et al., 2003) or substantial hatching success, metamorphosis, post-metamorphic sur- changes in temperature, salinity, pH, food levels, or dis- vival, and post-metamorphic growth. Salinity reduction solved oxygen concentrations (e.g., Hettinger et al., 2012; from 30 to 10 or 15 reduced relative hatching success, Li and Chiu, 2013; Bashevkin and Pechenik, 2015; Vander- presumably by reducing embryonic survival, but gener- plancke et al., 2015). For example, when larvae of the ally had no negative latent effects on juvenile survival or slipper snail Crepidula fornicata (Linnaeus, 1758) were starved for several days, the resulting juveniles grew sig- growth. Prolonged exposure to hypoxic conditions had no nificantly more slowly, even if the larval growth rates had negative effects, as seen on measurements recorded, returned to normal after larval feeding was resumed (Pech- other than abandonment of brood tubes by some females. enik et al., 1996, 2002). These effects were also observed There were no negative effects on days to emergence when larvae of C. fornicata were simply fed a less nutritious from brood tubes, numbers of larvae emerging from food source during larval development (Pechenik and brood tubes, juvenile survival, or juvenile growth. Future Tyrell, 2015). studies should consider the potential role of maternal Most of the studies that have documented such latent behavior in protecting embryos from at least short-term effects have focused on stressors experienced by larvae; few exposures to hypoxia, and the capacity for anaerobic have examined the extent to which subsequent juvenile or metabolism in both embryos and adults of this species. adult performance may be affected by stresses experienced during embryonic development. Although brooding or en- capsulation of embryos has often been thought of as pro- tective (Gillespie and McClintock, 2007 and Chaparro et Received 22 February 2016; accepted 14 June 2016. al., 2008, reviewed by Pechenik, 1979), under some cir- * To whom correspondence should be addressed. E-mail: jan.pechenik@ cumstances brooding can expose embryos to severe stress, tufts.edu resulting in measurable latent effects on post-metamorphic † Current address: Virginia Institute of Marine Sciences, College of William and Mary, Gloucester Point, Virginia 23062. development (e.g., Chaparro et al., 2014). For example, ‡ Current address: Department of Marine and Coastal Sciences, Rutgers periods of hypoxia (Segura et al., 2014) or severe salinity University, New Brunswick, New Jersey 08901. stress (Chaparro et al., 2014) experienced by brooded 103 This content downloaded from 139.070.105.159 on August 30, 2019 11:40:06 AM All use subject to University of Chicago Press Terms and Conditions (http://www.journals.uchicago.edu/t-and-c). 104 J. A. PECHENIK ET AL. embryos of the gastropod Crepipatella dilatata resulted in Materials and Methods significantly slower juvenile growth than that of brooded Collection and maintenance of adult specimens embryos that did not suffer such stresses. The mechanisms accounting for these such effects are poorly understood Capitella teleta broodstock were originally acquired in (Pechenik, 2006). 2012 from Dr. Judith Grassle of Rutgers University. A In this study we examined the short-term and latent population of adults was maintained at 20 °C in the lab effects of hypoxia and salinity stresses experienced by at Tufts University, using artificial seawater (ASW; In- brooded embryos of the salt marsh-dwelling, deposit- stant Ocean Spectrum Brands, Blacksburg, VA) at a feeding polychaete worm Capitella teleta Blake, Grassle, salinity of 30. Water was changed at least twice each and Eckalberger, 2009. After mating, females of C. teleta week, and worms were fed mud that had been collected deposit their developing embryos (maximum lengths Ͻ 300 from the Little Sippewissett Marsh in Falmouth, Massa- ␮m, Blake et al., 2009) on the interior wall of a specialized chusetts (Lat. 41.574556, Long. –70.636186). The mud was brood tube constructed by the mother from mucus and sand sieved through a 1-mm-filter to remove debris, then frozen grains (Grassle and Grassle, 1976; Biggers and Laufer, for several weeks before use (Cohen and Pechenik, 1999). 1999; Seaver et al., 2005; Blake et al., 2009); typically, at least 40 to 70 embryos are deposited per tube (Pechenik et Isolating embryos al., 2001b). The brood tubes are generally about 8 to 15 mm The laboratory population of Capitella teleta was visually long and about 0.6 to 1.3 mm wide (J. A. Pechenik, pers. inspected at least every other day for the presence of adult obs.). The female does not leave the brood tube for one to females in self-constructed brood tubes. Each brood tube several weeks (Pechenik and Cerulli, 1991; present study), was examined at 12ϫ, using a dissecting microscope to until her larvae escape into the plankton. The larvae are confirm the presence of embryos. Only brood tubes con- non-feeding lecithotrophs (Blake et al., 2009) and are ca- taining early embryos were used in the experiments, and pable of metamorphosing within 30 minutes of their release they were used within 24 h of their isolation. into the plankton (Butman et al., 1988; Dubilier, 1988; Pechenik and Cerulli, 1991). Metamorphosis is easily in- Salinity experiments: effects of embryonic exposure to low duced by providing fine sediment with high organic content salinity on hatching success, juvenile survival, and (Dubilier, 1988; Cohen and Pechenik, 1999). juvenile growth Populations of C. teleta are common in the shallow Three experiments were conducted to determine the im- mudflat areas of salt marshes and near sewage outflows and pact of pre-hatching exposure to reduced salinity on juve- nutrient-enriched fish farms (Levin et al., 1996; Blake et al., nile survival and growth, each testing the effects of a 2009), locations in which they are likely to periodically different exposure duration (24 h, 48 h, or 96 h). All encounter marked salinity fluctuation (Dubilier, 1988; Gray experiments were conducted at 20 °C. On the initial day of et al., 2002; Wu, 2002) and hypoxic conditions (typically Ϫ1 an experiment, adult populations were examined and the defined as oxygen concentrations below 2 ml O2 liter , requisite number of females with brood tubes were set aside. Diaz and Rosenberg, 2008). Salinity of 12 seems to be a For each experiment, brood tubes containing early embryos threshold for most stages of development of C. teleta; adults were haphazardly assigned to either the control (30) or the survived poorly and had reduced reproductive output at reduced-salinity group. In the first experiment, brood tubes reduced salinities of 10–12 (Levin et al., 1996; Pechenik et were exposed for 24 h to salinities of 30 (control), 25, 20, al., 2000); juveniles generally grew more slowly at salinities 15, or 10, with three replicates of one brood tube per salinity of 12–15 (Pechenik et al., 2000); and in short-term exper- level. The second and third experiments were conducted in iments (24–48 h), larvae became sluggish or stopped swim- the same way, except that brood tubes were exposed to ming at salinities of 10–12 (Pechenik et al., 2001b). Al- treatments, including the control, for 48 h and 96 h, respec- though prior studies with C. teleta have examined effects of tively. In all cases, each brood tube was held in a glass dish reduced salinity on larval survival, juvenile growth, and containing 50 ml of oxygenated seawater at the appropriate reproductive success (Pechenik et al., 2000, 2001a, b), none salinity.