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Edge-Drilling Behavior in the Predatory Gastropod Notocochlis Unifasciata

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Edge-Drilling Behavior in the Predatory Gastropod Notocochlis Unifasciata Vita Malacologica 13: 63-72 20 December 2015 Edge-drilling behavior in the predatory gastropod Notocochlis unifasciata (Lamarck, 1822) (Caenogastropoda, Naticidae) from the Pacific coast of Panama: taxonomic and biogeographical implications Alexis ROJAS Florida Museum of Natural History, Division of Invertebrate Paleontology, University of Florida, Gainesville, FL, 32611, USA; Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002, Balboa, Ancon, 0843-03092, Panama email: [email protected] Austin HENDY Natural History Museum of Los Angeles County, Los Angeles, CA, 90007, USA email: [email protected] Gregory P. DIETL Paleontological Research Institution, 1259 Trumansburg Road, Ithaca, NY 14850 USA; Department of Earth and Atmospheric Sciences, Cornell University, Ithaca, NY 14853 USA email: [email protected] (corresponding author) Key words: biological interactions, drilling predation, Central America ABSTRACT fossil and extant naticid predation have taken advantage of these highly quantifiable drilling traces in molluscan death We conducted a laboratory study to determine drillhole site- assemblages to study the ecology and evolution of naticids selectivity patterns in the predatory behavior of Notocochlis uni - and their prey (Kitchell, 1986; Kowaleswki, 2002; Kelley & fasciata (Lamarck, 1822), which is a common naticid gastropod Hansen, 2003). We still know very little, however, about how on the eastern Pacific coast of Central America, preying on two prey-capture behavior varies within and among naticid infaunal venerid bivalves – the thin-shelled and weakly orna - species in large part because research has focused on the mented Leukoma grata (Say, 1831) and the thick-shelled and traces of predation preserved on prey shells more than the strongly ornamented Iliochione subrugosa (Wood, 1828). Spatial behavior of the living organisms that produced them (Gonor, patterns of drillhole distribution indicate strong preferences for 1965; Kowalewski, 2002; Kelley & Hansen, 2003). drilling the umbonal region and the ventral edge of the shell, with By far the most common mode of naticid predation is the proportion of edge- to wall-drilling attacks increasing in drilling a hole through the wall of the prey’s shell, typically thicker, strongly ornamented prey that were larger than their near the umbo or center of the shell of bivalved prey (Negus, predator’s own size. Drilling patterns from museum and beach 1975; Rosewater, 1980; Vignali & Galleni, 1986; Ansell & samples of I. subrugosa collected across the geographic range of Morton, 1987; Dietl & Alexander, 1997; Alexander & Dietl, N. unifasciata (Panama to Costa Rica) were consistent with labo - 2001; Kingsley-Smith et al., 2003). A less well-known mode ratory findings. Review of the confirmed cases of edge-drilling of naticid predation is edge drilling, in which a predator drills behavior by other naticids indicates that this study is the first a hole at a point on the commissure between the closed valves confirmed report of the behavior in the naticid subfamily of a bivalved prey (Vermeij, 1980; Taylor, 1980; Ansell & Naticinae. In light of these findings, we discuss hypotheses on Morton, 1985; Vermeij & Roopnarine, 2001). Edge drilling the geography and ecology of edge-drilling predation by subtrop - takes less time than wall drilling because the prey’s shell is ical and tropical naticids to guide future research. typically thinnest at its margin, and is hypothesized to be advantageous in biologically hazardous environments where naticids face risks from enemies during the slow process of INTRODUCTION drilling prey (Vermeij & Roopnarine, 2001; Dietl et al., 2004; Dietl & Herbert, 2005). Naticid gastropods are important infaunal predators of Here we report on the drilling behavior of the naticid mollusks in marine soft-bottom communities worldwide that Notocochlis unifasciata (Lamarck, 1822) – formerly “ Natica drill a circular hole through their prey’s shell in order to feed unifasciata ”; see Appendix 1 – from Panama feeding on the (Kabat, 1990; Kelley & Hansen, 2003). Numerous studies on venerid bivalves Leukoma grata (Say, 1831) and Iliochione VITA MALACOLOGICA, 13: 63 Rojas, A. et al. – Drilling behavior of Notocochlis unifasciata weakly sculptured (cancellate) shell (Fig. 2B), whereas the shell of I. subrugosa is relatively smaller, thicker, more inflat - ed, and often strongly ornamented with rounded, commarginal folds (Fig. 2A) (Coan & Valentich-Scott, 2012). Each N. unifasciata specimen was kept separately in a 20 l tank with flow-through seawater maintained at 23.3˚-29.7˚C and 28.9-34.8 ppt. Each tank contained 5 cm of fine sand, which was sufficient for prey to maintain a shallow burrowing depth within 1 cm of the sediment surface as is typical for other venerids in life position (Stanley, 1970). Approximately 50 L. grata and I. subrugosa specimens were stored together in two separate 20 l holding tanks with 5 cm of fine sand and restocked periodically as prey were consumed by N. unifasci - ata predators. Potential prey fed on naturally occurring algae in the flow-through seawater system. After a 3-day acclima - tion period, three I. subrugosa and L. grata prey from the holding tanks were randomly selected from the range of sizes available and added to each N. unifasciata tank. The drilling activity of N. unifasciata predators was monitored daily, with Figure 1 . Map of southern Central America showing collecting locali - consumed prey in each tank replaced by a specimen of the ties. Geographic ranges of Iliochione subrugosa, Leukoma grata and same species and approximate size. Notocochlis unifasciata are shown in inset. CR = Costa Rica, PA = Panama. SITE SELECTIVITY OF BIVALVE PREY BY NOTOCOCHLIS UNIFASCIATA Drillhole site-selectivity by N. unifasciata on its bivalve subrugosa (Wood, 1828) under laboratory conditions. This prey was quantified using a landmark approach (Roopnarine geographically wide-ranging naticid species occurs on inter - & Beussink, 1999). All drilled specimens removed from the tidal mud- and sand-flats from Costa Rica to northern Peru laboratory tanks were digitally imaged using a standard pho - (Keen, 1971), where it preys on a diversity of gastropod and togrammetric protocol (Perea et al., 2008; Kolbe et al., 2011). bivalve prey (Gonor, 1965; Hughes, 1985). Our laboratory Four pseudolandmarks were selected on the exterior surface observations with N. unifasciata provide the first unequivocal of the valve to capture drillhole position: (1) the point of max - evidence of edge-drilling behavior in the genus Notocochlis . imum curvature of the ventral margin; (2) the point of maxi - We also discuss the role of prey morphology (shell thickness, mum curvature of the anterior margin; (3) the tip of the beak ornamentation and size) on edge-drilling behavior by N. uni - of the valve; and (4) the point of maximum curvature of the fasciata , provide evidence of edge drilling from beach-col - posterior margin. A fifth point corresponded with the drillhole lected and museum samples of I. subrugosa across the geo - itself. The selected points reflect the general external shape of graphic range of N. unifasciata , and outline hypotheses on the the valve, which is an important factor for naticid predators geography and ecology of edge-drilling predation by subtropi - when manipulating their prey (Kabat, 1990). The two-dimen - cal and tropical naticids to guide future research. sional landmark coordinates obtained for left valves were inverted to compare directly with the right valves (Kowalewski, 2004). The partial Procrustes superimposition MATERIAL AND METHODS method was used to remove effects of shell size from the analysis using landmarks 2 and 4 as a reference baseline. The LABORATORY OBSERVATIONS R function for landmark-based morphometrics developed by Thirty live specimens of N. unifasciata (13.2-40.0 mm in Claude (2008) was used to undertake this analysis. shell height (H)) were collected from intertidal habitats at Playa Farfan and Playa El Palmar near Panama City, Panama EFFECT OF BODY SIZE ON DRILLHOLE SITE (Fig. 1). Live prey specimens of both L. grata (~9-34 mm SELECTIVITY OF NOTOCOCHLIS UNIFASCIATA length (L)) and I. subrugosa (~12-30 mm L) were periodically To explore the effect of relative predator and prey size on collected from Bahia Bique (Fig. 1) throughout the duration of the drillhole site selectivity of N. unifasciata , both predator H the 2-month long study, which ran between April and May and L of L. grata and I. subrugosa prey were measured to the 2010 at the Smithsonian Tropical Research Institute’s Naos nearest 0.1 mm after each predation event observed in the lab - Island Laboratory in Panama City, Panama. These bivalve taxa oratory tanks. Predators and prey were binned into “small” < were selected because of their contrasting shell morphology, 20 mm and “large” ≥ 20 mm size classes to form four preda - which has been reported to influence the selection of a drilling tor / prey size ratio combinations: small predator / small prey; site by other tropical naticid species (Ansell & Morton, 1985). small predator / large prey; large predator / small prey; and Leukoma grata typically has a large, thin, relatively flat, and large predator / large prey. VITA MALACOLOGICA, 13: 64 Rojas, A. et al. – Drilling behavior of Notocochlis unifasciata Sample # wall- # edge- Locality name Locality ID Species Sample ID # valves source drilled drilled 31174 INB001479934 54 5 - 30265 INB001480878 11 1 4 31941 INB001483904 72 - 1 Museum Golfo
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