Drilling Predation Upon Ditrupa Arietina (Polychaeta: Serpulidae) from the Mid-Atlantic Açores, Portugal
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AÇOREANA, Suplemento 6, Setembro 2009: 157-165 DRILLING PREDATION UPON DITRUPA ARIETINA (POLYCHAETA: SERPULIDAE) FROM THE MID-ATLANTIC AÇORES, PORTUGAL Brian Morton & E.M. Harper Department of Zoology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK. E-mail: [email protected] Department of Earth Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EQ, UK. E-mail: [email protected] ABSTRACT A small, but significant proportion of the empty tubes of the free-living serpulid Ditrupa arietina dredged from the seabed off São Miguel, Açores, were punctured by small round holes. Analysis of these holes shows that they are typically single, made from the outside of the tube and located preferentially, suggesting that they represent the work of a predator. The likely identity of the predator is discussed but based on the co-occurrence in the dredges and the fact that most of the holes have a distinctive countersunk mor- phology, it is suggested that they were made by the small naticid Natica prietoi. If so, this study is the first record of such a predator/prey relationship. RESUMO Uma pequena mas significativa porção de tubos do serpulídeo livre Ditrupa arietina dragados do fundo marinho ao largo de São Miguel, Açores, estavam perfurados por pequenos orifícios redondos. Análise desses orifícios mostra que eles são tipicamente singulares, feito a partir do exterior do tubo e localizados preferencialmente, sugerindo que representam o trabalho de um predador. Discute-se a identidade provável do predador mas, com base na co-ocorrência nas dragagens e no facto de que a maioria dos orifícios possui uma distinta morfologia chanfrada, sugere-se que foram feitos pelo pequeno naticídeo Natica prietoi. Assim sendo, este estudo é o primeiro registo de tal relação predador/presa. INTRODUCTION In contrast, little appears to be known about predatory activities upon the tube- lthough polychaete worms are a dwelling Serpulidae (Polychaeta) despite Amajor source of food for a number of their cosmopolitan occurrence and fre- predatory taxa including fish, gastropods quently high abundance. There is, how- and birds, most of our knowledge is ever, observational evidence that gas- focused on predation of the larger errant tropods (Taylor & Morton, 1996; Tan & taxa. For example, amongst the predato- Morton, 1998), fish (Bosence, 1979; ry gastropods, representatives of the Witman & Cooper, 1983) and crustaceans Muricidae, Columbellidae, Fasciolariidae, (Bosence, 1979) feed on serpulids and, in Vasidae and Buccinidae as well as many the case of the buccinid gastropod Engina conoideans are specialist worm predators armillata (Reeve, 1846) in Hong Kong, (Pearce & Thorson, 1967; Taylor, 1978a, b, they are its prey of choice (Tan & Morton, 1980; Taylor et al., 1980; Shimek, 1984; 1998). Additionally, the development of Taylor & Lewis, 1995). Similarly, many calcareous tubes, a well-developed wading birds are specialist predators “fright response” (Poloczanska et al., upon intertidal endobenthic polychaetes 2004) and, in the case of encrusting (Goss-Custard, 1975). species, an often cryptic habit suggest 158 AÇOREANA 2009, Sup. 6: 157-165 that the evolution of the Serpulidae may figure 4) illustrate a living D. arietina in have been influenced by predation pres- its life position in the sediment. sure. Part of the problem in recognising The species has been recorded as a predatory activity on serpulid worms dominant member of soft-bottom com- undoubtedly results from their typically munities at depths of 100–250 metres in cryptic lifestyles that make direct obser- the Açores where the tubes of dead indi- vations difficult. Indirect methods to viduals also provide domiciles for the detect predatory activity on serpulids sipunculan worm Aspidopsiphon muelleri must rely on analyses of the predator’s Diesing, 1851 (Morton & Britton, 1995; gut contents to recognise setae (Taylor & Morton & Salvador, 2009). Morton, 1996) or the identification of any characteristic damage to the tube caused MATERIALS AND METHODS by a predator, although for many preda- tors, for example E. armillata, which was During July 2006, large numbers of recorded feeding via the prey’s aperture the serpulid polychaete Ditrupa arietina (Tan & Morton, 1998), no such character- were collected from depths of between istic damage results. 50-200 metres off Vila Franca do Campo, In this paper we describe drill holes São Miguel, Açores. The samples were made in the tube of the endobenthic ser- collected and processed as reported in pulid Ditrupa arietina (Müller, 1776) from Morton & Salvador (2009). Following ini- the subtidal seabed off the island of São tial observations that some tubes were Miguel in the Açores (Portugal). We pre- perforated by drill holes, the tubes of sent evidence that these are the result of dead individuals were separated and predation and further discuss evidence inspected for evidence of such drilling. as to the likely culprit(s). For each holed tube, the following data were collected: tube length to the nearest Ditrupa arietina (Müller, 1776) 1 mm using vernier callipers, number of drillholes per tube and the morphology of Ditrupa arietina is a widespread the drillhole. Further observations were endobenthic serpulid worm, common in made on the morphology of the drillholes the Mediterranean where it achieves of a small number of specimens by scan- high densities and there is evidence in ning electron microscopy (SEM). These some areas that its abundance is increas- specimens were prepared by cleaning in ing (Gremare et al., 1998a, b; Bolam & an ultrasonic bath prior to mounting Fernandes, 2002; Labrune et al., 2007). them, coated in gold, for SEM (JEOL 820 – The worm secretes a curved, tusk- University of Cambridge). shaped, calcareous tube up to 23 mm Finally, the mean tube lengths plus long and about 3 mm across at its widest standard deviations of intact living indi- point. It lives within the sediment, the viduals of Ditrupa arientina and those narrowest posterior end down, with an with drill holes were compared using a anterior bulge (about 10% of the tube) t-test. exposed above the substratum. This anterior bulge houses the circlet of twen- RESULTS ty feeding tentacles when they are retracted and the anterior aperture is Holed individuals of Ditrupa arietina sealed by a further tentacle bearing an were identified from each of the six sam- operculum. Morton & Salvador (2009, pling stations, described by Martins et al. MORTON & HARPER: DRILLING PREDATION UPON DITRUPA ARIETINA 159 (2009), but no significant differences in numbers were obtained between them with regard to the incidence of drilled tubes (see Morton & Salvador, 2009 for details). In total 5,453 tubes of D. arietina were retrieved and examined and from which we identified 104 fragments and intact empty tubes with holes in them, that is, approximately 1.9% of all empty tubes examined. The vast majority of the tubes were perforated by a single drill- hole but a few had two or even three com- plete holes. No incomplete holes were observed nor any that showed signs of repair or healing by the occupant. All were drilled perpendicular to the surface FIGURE 1. Scanning electron micrographs of a of the tube and were clearly produced variety of drill holes in the tubes of Ditrupa ari- from the outside, as evidenced by a wider etina collected from the seabed offshore from outer diameter. Vila Franca do Campo, São Miguel, Açores, in All holes in the tubes of Ditrupa arieti- 2006. Scale bars represent 100 µm for A and B na were small, with an outer diameter of and 200 µm C and D. less than 700 µm. In outline, the perfora- tions were mostly circular (Figure 1A, B) but a few were more elliptical (Figure 1C). The outer edges of the drillholes were clearly defined, and SEM observations of the surface of the tube adjacent to the hole show no obvious signs of either dissolu- tion or rasping. The inner perforations were rather more ragged and smaller than the outer diameter. Most of the holes we have examined had curved walls lead- ing to a countersunk morphology, although some (Figure 1D) were more straight-sided. FIGURE 2. Histograms showing the size dis- The positions of drill holes in the tributions (tube lengths) of living (white) and tubes of Ditrupa arietina are shown in drilled (black) individuals of Ditrupa arietina Figure 2. It is clear that most are located collected from the seabed offshore from Vila in the mid portion of the tube, below the Franca do Campo, São Miguel, Açores, in 2006. anterior bulge. Although they occur all around the circumference of the tube, the distribution of the holes is not uniform, there being a clear preference for the con- plotted together with the same data for cave aspect. drilled individuals in Figure 3. Although The length distributions of a sub-sam- virtually all sizes of D. arietina tubes were ple (n = 376) of living Ditrupa arietina drilled (from 5-21 mm tube lengths), the recorded by Morton & Salvador (2009) are mean length of the drilled D. arietina 160 AÇOREANA 2009, Sup. 6: 157-165 tubes (n = 102) was 12.7 (S.D. 4.3) where- An obvious question to try and as that of the tubes occupied by living D. address is the identity of the drilling arietina (n = 378) was 14.9 (S.D. 2.8). The predator(s). A wide array of predatory result of the t-test showed that the means taxa, including several species of gas- of the two samples were significantly dif- tropods, cephalopods, and worms, are ferent (p = <0.05), suggesting that drilled known to be able to drill holes in the individuals were smaller. skeletons of their prey items (Kabat, 1990). However, as noted by Bromley (1981), it is notoriously difficult to assign drillholes, with any degree of certainty, to a particular creator.