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Gastropoda: Velutinidae), a Specialist Predator of Ascidians

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Gastropoda: Velutinidae), a Specialist Predator of Ascidians Canadian Journal of Zoology The life history and feeding ecology of velvet shell, Velutina velutina (Gastropoda: Velutinidae), a specialist predator of ascidians Journal: Canadian Journal of Zoology Manuscript ID cjz-2018-0327.R1 Manuscript Type: Article Date Submitted by the 03-Jun-2019 Author: Complete List of Authors: Sargent, Philip; Northwest Atlantic Fisheries Centre, Fisheries and Oceans Canada Hamel, Jean-Francois; Society for the Exploration and Valuing of the EnvironmentDraft Mercier, Annie; Memorial University of Newfoundland, Ocean Sciences Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Velutina velutina, velvet shell, velutinid, gastropod, invasive species, Keyword: specialist predator, ascidian https://mc06.manuscriptcentral.com/cjz-pubs Page 1 of 42 Canadian Journal of Zoology 1 The life history and feeding ecology of velvet shell, Velutina velutina (Gastropoda: Velutinidae), a specialist predator of ascidians P. S. Sargent*, J-F. Hamel, and A. Mercier P. S. Sargent1 Department of Ocean Sciences, Memorial University, St. John’s (Newfoundland and Labrador) Canada A1C 5S7 Email: [email protected] J-F Hamel Society for the Exploration and ValuingDraft of the Environment (SEVE), Portugal Cove-St. Philips (Newfoundland and Labrador) Canada A1M 2B7 Email: [email protected] A. Mercier Department of Ocean Sciences, Memorial University, St. John’s (Newfoundland and Labrador) Canada A1C 5S7 Email: [email protected] * Corresponding Author: Philip S. Sargent Department of Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, 80 East White Hills Road, St. John’s, Newfoundland and Labrador, Canada, A1C 4N1 Email: [email protected] Phone: 1 (709) 772-4278 Fax: 1 (709) 772-5315 1 Current Contact Information for P. S. Sargent: Department of Fisheries and Oceans Canada, Northwest Atlantic Fisheries Centre, 80 East White Hills Road, St. John’s, Newfoundland and Labrador, Canada, A1C 4N1 Email: [email protected] https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 2 of 42 2 The life history and feeding ecology of velvet shell, Velutina velutina (Gastropoda: Velutinidae), a specialist predator of ascidians P. S. Sargent*, J-F. Hamel, and A. Mercier Abstract Velvet shell, Velutina velutina (O. F. Müller, 1776), is a specialist predator of ascidians, like other members of the gastropod family Velutinidae. Globally, invasive ascidians have become problematic, ecologically and economically, yet ecological knowledge of velutinids remains limited. This study outlines the life history and feeding ecology of V. velutina in eastern CanadaDraft based on laboratory work complemented by field observations. The life history of V. velutina is closely linked with ascidians, which serve as prey and protection for their egg capsules. Egg capsules were embedded within tunics of Aplidium glabrum (Verrill, 1871) and Ascidia callosa Stimpson, 1852, but the latter was preferred. Seasonal behavioural shifts were consistent annually and corresponded with seawater temperature cycles. Feeding dominated during the coldest months (January – May), growth occurred as water temperature increased to the annual maximum (June and July), transitioned to mating during the warmest period (July/August), and egg capsule deposition dominated as water temperature declined (November – January). Larvae hatched between January and July after 2 – 4 months of development. Velvet shell preyed on all ascidian species presented during this study, including golden star tunicate, Botryllus schlosseri (Pallas, 1766), and vase tunicate, https://mc06.manuscriptcentral.com/cjz-pubs Page 3 of 42 Canadian Journal of Zoology 3 Ciona intestinalis (Linnaeus, 1767), two non-indigenous species, although solitary species were preferred. Keywords Velutina velutina, velvet shell, velutinid, gastropod, invasive species, specialist predator, ascidian Introduction Members of the gastropod family Velutinidae (formerly Lamellariidae) are specialized predators of ascidians that closely associate with their prey (Fretter and Graham 1962; Ghiselin 1964; Behrens 1984; Dias and Delboni 2008) and deposit their egg capsules within the tunic of ascidiansDraft (Diehl 1956; Strathmann 1992; Page 2002; Dias and Delboni 2008). The close association of velutinids and ascidians has even been described as a symbiotic (sensu lato) relationship (Queiroz and Sales 2016). Available literature on velutinids consists primarily of anatomical and taxonomical descriptions (e.g. Gulbin and Golikov 1997; 1999), observational references to biogeography, depth distributions, and habitat associations (e.g. Fretter and Graham 1981; Gulbin 2005). Scarcity of ecological and biological information on velutinids may be due in part to their cryptic nature and the fact that few specimens have ever been collected (Lambert 1980). The mantle of most velutinid species partially or completely covers a thin and weakly calcified shell (Gulbin and Golikov 1997) and often mimics the colour and texture of the tunic of ascidians (Ghiselin 1964; Lambert 1980; Behrens 1984). This renders velutinids almost indistinguishable from their prey (Ghiselin 1964; Behrens 1980; Lambert 1980). Furthermore, velutinids are commonly misidentified as dorid nudibranchs (Jeffreys 1867; Behrens 1984; Dias and Delboni 2008) and some https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 42 4 species are nocturnal, remaining concealed during the day (Sarma and Pattanaik 1986). In general, our understanding of the ecological role of velutinids in subtidal communities is limited. The velvet shell, Velutina velutina (O. F. Müller, 1776), is one of the most common and widely distributed velutinid species in northern seas (Derjugin 1950). It is a sublittoral species with a boreal-arctic distribution (Gulbin and Golikov 1999; Gulbin 2005) found to depths of 1000 m (Fretter and Graham 1981; Gulbin 2005). In the northwest Atlantic, this species extends from the Arctic to as far south as Cape Cod (Massachusetts, USA) but becomes increasingly rare and occurs deeper towards its southern range (Fretter and Graham 1981). Members of the genus Velutina have an external shell and the mantle may onlyDraft cover a portion of the shell’s surface along the edge of the aperture (Fretter and Graham 1981). To our knowledge, the only ecological studies of V. velutina were conducted in northern Europe and examined predation on and egg deposition in the ascidian Styela coriacea (Alder and Hancock, 1848) (Diehl 1956), copulation (Diehl 1956), and planktonic larval development (Lebour 1935; Thorson 1946; Mileikovsky 1960; Fretter and Pilkington 1970; Thiriot-Quiévreux 1974). A better understanding of the ecology of velutinids would not only increase our knowledge of this poorly understood gastropod family but may also be relevant to the control of some aquatic invasive species. Non-indigenous ascidians have proven to be very successful invasive species globally (Lambert 2007). Invasive ascidians may have significant impacts both ecologically, by altering community structure (Lambert and Lambert 2003; Valentine et al. 2007), and economically, by fouling man-made structures, especially shellfish aquaculture infrastructure (Carver et al. 2003; LeBlanc et al. 2007; https://mc06.manuscriptcentral.com/cjz-pubs Page 5 of 42 Canadian Journal of Zoology 5 Rocha et al. 2009). Yet, knowledge of biotic resistance of benthic marine communities to such invasions is lacking (Lambert 2007; Epelbaum et al. 2009). Determining the response of benthic communities to invasive species (e.g. presence and role of potential predators such as velutinids) is crucial to understand and mitigate species invasions. The purpose of the present study was to investigate the life history and feeding ecology of V. velutina and provide insight into the role of velutinids within the subtidal communities they inhabit. It combined laboratory studies complemented by field observations to determine diet and feeding habits (preferences, rates, and periodicity) as well as seasonal behavioural patterns. Mating, egg laying, larval development and hatching were characterized and the role of environmental factors in the control of these behaviours were also examined. As Drafta specialist predator of ascidians, V. velutina may represent a natural means of mitigating the impacts of some non-indigenous ascidians. Materials and methods Collections and field sites Most field observations and collections of V. velutina were made opportunistically (77.8% of dives) while conducting dives for other purposes. Field observations of habitat associations and behaviours of V. velutina were recorded2 and used to complement observations recorded in the laboratory. Over the course of 41 dives (mean = 36 min dive time) conducted between November 2005 and August 2011 around insular Newfoundland, 105 velutinids were observed and 75 individuals were collected and transferred to Memorial University’s Oceans Science Centre3. Five additional 2 as per Table S1 and S2, respectively 3 Tables S1 and S3 https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 6 of 42 6 individuals were collected over four dives between March and May 2017 (mean = 44 min dive time) and transferred to the Northwest Atlantic Fisheries Centre3. In 2006 and 2007, samples of callused tunicate, Ascidia callosa Stimpson, 1852, were collected from two sites4 and examined for the presence of developing or previously hatched egg capsules
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