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Reproductive Biology of the Antarctic ''Sea Pen'' Malacobelemnon Daytoni (Octocorallia, Pennatulacea, Kophobelemnidae)

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Reproductive Biology of the Antarctic ''Sea Pen'' Malacobelemnon Daytoni (Octocorallia, Pennatulacea, Kophobelemnidae) RESEARCH/REVIEW ARTICLE Reproductive biology of the Antarctic ‘‘sea pen’’ Malacobelemnon daytoni (Octocorallia, Pennatulacea, Kophobelemnidae) Natalia Servetto,1,2 Luciana Torre1,2 & Ricardo Sahade1,2 1 Instituto de Diversidad y Ecologı´a Animal, Facultad de Ciencias Exactas, Fı´sicas y Naturales, Universidad Nacional de Co´ rdoba, Av. Ve´ lez Sa´ rsfield 299 (X5000JJC), Co´ rdoba, Argentina 2 Consejo Nacional de Investigaciones Cientı´ficas y Tecnolo´ gicas, Av. Ve´ lez Sa´ rsfield 1611 (X5000HVA), Co´ rdoba, Argentina Keywords Abstract Antarctica; benthic communities; Pennatulacea; reproduction; oogenesis. The reproductive biology of the sea pen Malacobelemnon daytoni was studied at Potter Cove, South Shetland Islands, where it is one of the dominant species in Correspondence shallow waters. Specimens collected at 15Á22 m depth were examined by Ricardo Sahade, Instituto de Diversidad y histological analysis. M. daytoni is gonochoristic and exhibited a sex ratio of 1:1. Ecologı´a Animal, Facultad de Ciencias Oocyte sizes (300 mm) and the absence of embryos or newly developed Exactas, Fısicas y Naturales, Universidad ´ larvae in the colonies suggest that this species can have lecithotrophic larvae Nacional de Co´ rdoba, Av. Ve´ lez Sa´ rsfield 299 (X5000JJC), Co´ rdoba, Argentina. and experience external fertilization. This life strategy is in line with other E-mail: [email protected] members of the group and supports the hypothesis that this could be a phylogenetically fixed trait for pennatulids. It was observed that oocytes were generated by gastrodermic tissue and released to the longitudinal canal. Thereafter, they migrate along the canal until they reach maturity and are released by autozooids at the top of the colonies. This striking feature has not yet been reported for other pennatulaceans. Mature oocytes were observed from colonies of 15 mm in length, suggesting that sexual maturity can be reached rapidly. This is contrary to what is hypothesized for the vast majority of Antarctic benthic invertebrates, namely that rates of activities associated with development, reproduction and growth are almost universally very slow. This strategy may also explain the ecological success of M. daytoni in areas with high ice impact as in the shallow waters of Potter Cove. Antarctic benthic communities are often characterized octocorals (Brito et al. 1997; Orejas et al. 2002; Orejas and dominated by epibenthic suspension feeders such as et al. 2007). sponges, bryozoans, cnidarians and ascidians (Arntz et al. Octocorals are important members of benthic ecosys- 1994; Starmans et al. 1999; Gili et al. 2006). Information tems worldwide. They are found in marine habitats from on the reproductive biology of the species is essential to intertidal to abyssal waters and are distributed from the understanding the population dynamics and potential Arctic to the Antarctic (Bayer 1973). Although they have responses to disturbances. Despite some information that been intensively studied worldwide, reproductive traits exists on reproductive traits of Antarctic suspension of the group are scarcely reported. Among octocorals, the feeders such as echinoderms, bryozoans, brachiopod, order Pennatulacea (sea pen) is represented by 35 genera ascidians and bivalves, among others (Gutt et al. 1992; with approximately 200 species (Williams & Cairns 2005; Poulin & Fe´ral 1996; Barnes & Clarke 1998; Meidlinger Williams 2011). Sea pens are generally adapted to living et al. 1998; Sahade et al. 2004; Strathmann et al. 2006; in soft sediment habitats. They are formed by a modified Kang et al. 2009; Rodrı´guez et al. 2013), only one piece and persistent primary polyp (oozooid) and by the of work has focused on deep-water scleractinians (Waller muscular peduncle responsible for anchoring the colony et al. 2008) and a few studies have been devoted to in the sediment, while the rachis bears the autozooids Polar Research 2013. # 2013 N. Servetto et al. This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial 3.0 1 Unported License (http://creativecommons.org/licenses/by-nc/3.0/), permitting all non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Citation: Polar Research 2013, 32, 20040, http://dx.doi.org/10.3402/polar.v32i0.20040 (page number not for citation purpose) Reproductive biology of the Antarctic ‘‘sea pen’’ N. Servetto et al. and siphonozooids. The latter have cilia and are known pennatulid M. daytoni and the bivalve Laternula elliptica to generate currents, whereas autozooids are responsible significantly increased, while the abundance of other for feeding and potentially have reproductive functions, species, especially the ascidians Molgula pedunculata and the latter usually depending on their position in the Cnemidocarpa verrucosa diminished (Sahade et al. 1998; colony (Bayer et al. 1983; Williams 1995). Sahade et al. unpubl. data). The dramatic shift observed in Despite the limited knowledge of the biology, especially the benthic shallow community of Potter Cove is remark- the reproductive traits of the order, some characteristics of able, and so is the fact that L. elliptica and M. daytoni the reproductive strategies have been studied in some dominate in a depth range highly impacted by ice. species, including gametogenesis, temporal patterns and L. elliptica is able to bury down 50 cm into the sediment. synchronicity of oogenesis (Chia & Crawford 1973; Rice Although many pennatulids are also able to bury into et al. 1992; Eckelbarger et al. 1998; Soong 2005; Edwards the sediment, divers did not observe this behaviour in & Moore 2008, 2009; Pires et al. 2009). All studied sea M. daytoni. This suggests that this species must present a pens are gonochoristic and broadcast spawners. Gametes high population turnover to cope with the impact are released and fertilized externally and probably de- of ice. This strategy is not common and has not been velop into lecithotrophic larvae, either nourishing just reported for Antarctic invertebrates (Clarke 1996; Po¨rtner from egg reserves or including zooxanthellae products. 2002). These observations suggest that these may be phylogen- The aim of the present work was to study the repro- etically fixed characteristics for Pennatulacea. However, ductive biology of M. daytoni. It was first tested whether only a scarce number of species was examined and other gonochorism and broadcast spawning are characteristic coral groups (i.e., scleractinians or the more related for a small-body-sized Antarctic species. This may support alcyonacean octocorals) show high plasticity: gonochor- or disprove the hypothesis that gonochorism and broad- ism and hermaphroditism, broadcast spawners and broo- cast spawning are fixed reproductive traits in Pennatula- ders, unisexual parthenogenic or even autotomy of small ceans. Second, it was assessed whether the reproductive fragments with root-like processes have been observed biology of this species may explain its ecological success in (Dahan & Benayahu 1997a, b; McFadden et al. 2001; the Potter Cove ecosystem. Orejas et al. 2002; Orejas et al. 2007). The latitudinal trend from broadcast spawning to brooding in several marine invertebrate species is an Materials and methods aspect among a series of biological traits also known as the Thorson’s Rule (Mileikovsky 1971). Although Thorson’s Study site and sampling Rule has been challenged and misinterpreted several The study was carried out at Potter Cove, King George times (see Pearse et al. 1991; Arntz & Gili 2001), it seems Island (Isla 25 de Mayo), South Shetland Islands, where to be exhibited by some scleractinians and octocorals the Antarctic Argentine Station Carlini and the (Coma et al. 1995; Waller et al. 2008). In addition, large ArgentineÁGerman Dallmann Laboratory are located colony, or module, size has been related to external (62814’S, 58838’W; Fig. 1). fertilization, while brooding has been related to small Specimens of Malacobelemnon daytoni were collected size in octocorals. This relationship can be direct, due to monthly by scuba diving over the period January 2009Á isometric constraints as suggested for individual species, December 2010. Specimens were collected at 15Á22 m or indirect, as responses to environmental physical depth and transported to the surface in a metal cage to factors. Brooding, in turn, could facilitate the hermaph- avoid damaging the colonies. The total length of each roditism observed in several species, including octocorals individual, from base to tip, was measured and preserved (Strathmann et al. 1984; McFadden et al. 2001). There- in 4% formalin for histological purposes. Fixed indivi- fore, information on the reproductive biology of the duals were rinsed with fresh water, after the rods were Antarctic sea pen Malacobelemnon daytoni is important in decalcified in diluted HNO3; they were then embedded in order to test if gonochorism and broadcast spawning are paraffin. Thereafter, the material was serially sectioned phylogenic constraints in pennatulids. and stained with Hematoxilin-Eosin for histological At Potter Cove, South Shetland Islands, a shallow examination. Antarctic benthic community dominated by a sea pen Longitudinal histological cuts of the colonies were species was documented (Sahade et al. 1998). The sea pen examined under a stereomicroscope. Females and was later described as the new species Malacobelemnon males were readily distinguishable and separated. In daytoni
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