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<I>Chelonibia Testudinaria</I>

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<I>Chelonibia Testudinaria</I> Bull Mar Sci. 90(2):581–597. 2014 research paper http://dx.doi.org/10.5343/bms.2013.1033 Substratum fidelity and early growth in Chelonibia testudinaria, a turtle barnacle especially common on debilitated loggerhead (Caretta caretta) sea turtles 1 Department of Biology, College Kelly Sloan 1 * of Charleston, Charleston, South John D Zardus 2 Carolina 29424. Martin L Jones 3 2 The Citadel, Department of Biology, 171 Moultrie Street, Charleston, South Carolina 29409. ABSTRACT.—The barnacle, Chelonibia testudinaria 3 College of Charleston, (Linnaeus, 1758), is reported to associate with nearly Department of Mathematics, every species of sea turtle and is particularly common 66 George Street, Charleston, on loggerheads, Caretta caretta (Linnaeus, 1758), with South Carolina 29424. symptoms of Debilitated Turtle Syndrome (DTS). Here, we * Corresponding author email: test recruitment rates of C. testudinaria on various natural <[email protected]>. and artificial substrata, including carapace from healthy and Present address: Sanibel-Captiva debilitated loggerheads. In addition, the sizes of individual Conservation Foundation 3333 barnacles were followed through time to estimate early Sanibel-Captiva Road, Sanibel, Florida 33957. growth rates and to provide attachment duration estimates. Floating racks holding replicate panels of four treatments (DTS turtle carapace scutes, healthy turtle carapace scutes, Plexiglas®, and slate tile) were placed at four independent sites in Charleston County, South Carolina. Panels were monitored for 34–54 d. Our findings indicate that C. testudinaria larvae recruit and grow at significantly higher rates along the open shore vs protected areas, but do not recruit differentially to the four substratum types. Individual barnacle growth was highly variable within and between sites and substratum types; the mean growth rate was 4.28 mm d−1 (95% CI: 3.42–5.14 mm d−1). However, due to the high variability in growth, this value cannot serve as a fine-scale indicator for attachment duration. Further experiments of Date Submitted: 10 April, 2013. Date Accepted: 11 October, 2013. substratum selection and long-term survival are needed to Available Online: 20 February, 2014. fully clarify the nature of the barnacle/turtle association. Substratum selection by marine invertebrate larvae is specific for a number of ses- sile species (Pawlik 1992). For these organisms, there is strong selection to locate appropriate habitat during the larval period because it leads to survival and repro- duction at the adult stage (Pasternak et al. 2002, Railkin 2004). Acorn barnacles (Cirripedia: Thoracica: Balanomorpha) are sessile organisms that exhibit varying de- grees of substratum specificity across species, ranging from those that are generalists to others that are highly selective (Southward 1987, Anderson 1994). Epibiotic bar- nacles in particular exhibit distinct settlement preferences, with species from several different families attaching exclusively to a single host organism such as sponge (e.g., Archaeobalanidae), coral (e.g., Pyrgomatidae), or crustacean (e.g., Poecilasmatidae) (Molenock and Gomez 1972, Anderson 1992, Voris et al. 1994, Van Syoc and Winther 1999, Mokady and Brickner 2001, Tsang et al. 2009). The whale and turtle barnacles Bulletin of Marine Science 581 © 2014 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 582 Bulletin of Marine Science. Vol 90, No 2. 2014 (superfamily Coronuloidea) are especially remarkable for attaching to hosts that are mobile (Darwin 1854, Monroe 1981, Scarff 1986, Zardus and Balazs 2007). Nearly all species of barnacles undergo planktic larval development during which settlement is preceded by a period of dispersal of the larvae in the environment fol- lowed by delivery to a substratum. Larval dispersal and transport are key compo- nents of settlement and involve many factors which, depending on location, may include winds (Thiébaut et al. 1994, Bertness et al. 1996, Epifanio and Garvine 2001), currents and tides (Johnson 1960, Scheltema 1968, 1971, Efford 1970, Epifanio 1988), bathymetric distribution (vertical displacement) of larvae due to hydrodynam- ics (Pineda et al. 2007), salinity (Thiébaut et al. 1992), larval abundance (Raimondi 1990), and larval behavior (reviewed in Pineda et al. 2007). Vagaries in these factors contribute to large-scale spatial variability in settlement patterns (Gaines et al. 1985, Pineda 2000, Raimondi 1990). Epibiotic specialists such as turtle and whale barna- cles face the additional challenge of locating a scarce and mobile substratum, raising the question of how they find such specialized substrata. The larval settlement stage of barnacles, the cyprid, does not feed but instead acquires the energy reserves needed to power the search for suitable substratum from its earlier feeding stages (nauplius I–VI) (Lucas et al. 1979, Walker et al. 1987, Thiyagarajan et al. 2002). Consequently, the search period is finite, but its maximum duration is difficult to predict (Hentschel and Emlet 2000). For some species it is known that the cyprid stage can persist for as long as 3–4 wks (Lucas et al. 1979). The role of the timing of larval settlement on juvenile growth is considered species specific (Thiyagarajan et al. 2003), but prolonged larval life leads to limited energy reserves and can result in failure to metamorphose and decreased substratum speci- ficity (Pechenik et al. 1993, Jarrett 2003, Thiyagarajan et al. 2003). Upon finding a substratum, environmental factors including light, boundary currents, gravity, hy- drostatic pressure, temperature, and salinity can be important cues directing cyprid attachment (Crisp 1984), along with surface texture (Crisp and Barnes 1954) and substratum properties such as hardness and wettability (Roberts et al. 1991). In ad- dition, chemical constituents from the substratum, from conspecifics, and from mi- crobial biofilms also play a role in site selection and adhesion (Crisp and Ryland 1960, Crisp and Meadows 1963, Jarrett 1997, Qian et al. 2003, Zardus et al. 2008, Elbourne and Clare 2010, Thiyagarajan 2010, Holm 2012). Though known to aid settlement in at least one epibiotic barnacle (Standing et al. 1984), chemical cues have not been well studied in commensal species. Barnacles that are obligate epizoites of sea turtles range from several species that are specialized for particular turtle species (Frick et al. 2011, Frick 2012, Hayashi 2013) to Chelonibia testudinaria (Linnaeus, 1758), which lives on all species of sea turtles (Frick et al. 1998, Kitsos et al. 2003, Lazo-Wasem et al. 2011), as well as on crabs and other crustaceans (Cheang et al. 2013) and sirenians (Zardus et al. 2014). The effects of barnacles on turtles are not well documented, but these crustaceans are considered commensals rather than parasites as they draw no nutritional en- ergy from their hosts nor do they provide any known benefits (Zardus et al. 2007). However, they are sometimes associated with wounds (Flint et al. 2009) and in high abundance barnacles may impose negative effects by increasing frictional drag on their hosts. Chelonibia testudinaria is the largest of the turtle barnacles; it typically grows on the scutes of the carapace and plastron of sea turtles, but has also been found on scales Sloan et al.: Substratum fidelity and early growth inChelonibia testudinaria 583 of the head and flippers and occasionally on the claws (Matsuura and Nakamura 1993, Pfaller et al. 2006). The anatomical features (scutes, scales, and claws) are protected from the outside environment by a superficial layer of keratinized tissue (Block and Bolling 1938, Espinoza et al. 2007) and it is possible that the protein composition of the keratin is recognized by C. testudinaria cyprids. Recent studies have established that Chelonibia patula (Ranzani, 1818), C. testudinaria (Cheang et al. 2013), and Chelonibia manati Pilsbry, 1916 are the same species (Zardus et al. 2014). Although C. testudinaria has historically been considered to associate only with sea turtles, these studies reveal that it also occurs on the skin of snakes, carapaces of arthropods, and the epidermis of sirenians. Chelonibia testduinaria is particularly common on loggerhead sea turtles, Caretta caretta (Linnaeus, 1758), in coastal waters of the southeastern US (Dodd 1988, Frick and Slay 2000). Specifically, the carapaces of many juvenile loggerheads exhibiting symptoms of Debilitated Turtle Syndrome (DTS) are almost completely covered with C. testudinaria (Norton et al. 2008) and the soft tissue is typically encrusted with an- other barnacle, Platylepas hexastylos (Fabricius, 1798) (KS pers obs). In recent years, DTS has accounted for an increasing percentage of loggerhead strandings in South Carolina (mean = 13.7% of total loggerhead strandings from 2000 to 2011; South Carolina Department of Natural Resources unpubl data) and has become a growing concern for sea turtles in the Southeastern United States. Turtles exhibiting symp- toms of DTS are characteristically emaciated, anemic, hypoglycemic, and are often completely covered in barnacles when they strand. The heavy epibiota load associated with DTS is likely the result of a multifactorial process. Debilitation results in stationary floating and decreased grooming, which likely facilitates cyprid attachment. Healthy C. caretta reduce epibiont loads by ac- tively scraping the carapace against hard substrata (Frick and McFall 2007). Excessive stationary floating due to debilitation may place
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