ICES Journal of Marine Science (2011), 68(2), 399–407. doi:10.1093/icesjms/fsq066 The association between a deep-sea gastropod Pedicularia sicula (Caenogastropoda: Pediculariidae) and its coral host Errina dabneyi (Hydrozoa: Stylasteridae) in the Azores Andreia Braga-Henriques1*, Marina Carreiro-Silva1, Filipe M. Porteiro1, Valentina de Matos 1, ´Iris Sampaio1, Oscar Ocan˜a2, and Se´rgio P. A´vila3 1IMAR/DOP-UAz, Department of Oceanography and Fisheries, University of the Azores, 9901-862 Horta, Portugal 2Departamento de Biologı´a Marina, Fundacio´n Museo del Mar, Autoridad Portuaria de Ceuta, Muelle Can˜onero Dato S/N 51001, North Africa 3Department of Biology and CIBIO, University of the Azores, Rua da Ma˜e de Deus, Apartado 1422, 9501-801 Ponta Delgada, Portugal Downloaded from https://academic.oup.com/icesjms/article/68/2/399/614681 by guest on 23 September 2021 *Corresponding Author: tel: +351 292 207800; fax: +351 292 207811; e-mail: [email protected]. Braga-Henriques, A., Carreiro-Silva, M., Porteiro, F. M., de Matos, V., Sampaio,´ I., Ocan˜a, O., and A´vila, S., P. 2011. The association between a deep-sea gastropod Pedicularia sicula (Caenogastropoda: Pediculariidae) and its coral host Errina dabneyi (Hydrozoa: Stylasteridae) in the Azores. – ICES Journal of Marine Science, 68: 399–407. Received 31 August 2009; accepted 8 April 2010; advance access publication 30 June 2010. The Azores region harbours the richest communities of stylasterid corals in the Northeast Atlantic area. Of the nine deep-water species found there, Errina dabneyi seems to be the most abundant species; it is commonly collected as bycatch from longline fishing. E. dabneyi host Pedicularia gastropods on their branches, and a detailed study of shell shape and morphometry at different growth stages, complemented by shell characterization through scanning electron microscopy, allows the individuals to be identified as Pedicularia sicula. The incidence of this species on E. dabneyi was high (69.8%), with abundances ranging between 1 and 223 indi- viduals per colony. The pediculariids exhibited a high degree of plasticity and produced evident traces on the stylasterid skeletons at their fixation points, suggesting that they are ectoparasites and not predators of E. dabneyi. The stylasterid colonies also hosted a rich associated fauna dominated by suspension-feeders using the coral as substratum and for protection. Keywords: Azores, cold-water corals, parasitism, Pedicularia, Pediculariidae, Stylasteridae, symbiont. Introduction stylasterids, which appear widely distributed throughout insular The genus Pedicularia Swainson, 1840 (Caenogastropoda: areas (Cairns, 1992), this species is known to occur only in the Pediculariidae) encompasses 10 gastropod species (Simone, Azores and the Mid-Atlantic Ridge southwest of the Azores, 2005; Lorenz and Fehse, 2009), commonly reported as symbionts mainly at upper bathyal depths (Zibrowius and Cairns, 1992). It of stylasterid corals (Zibrowius and Cairns, 1992; Bouchet and possesses a uniplanar fan-shaped calcified skeleton up to 40 cm Ware´n, 1993; Goud and Hoeksema, 2001). Many gastropods high and wide with a reticulate-granular texture, which is living in association with corals are described in the literature as covered by a thin layer of tissue (Zibrowius and Cairns, 1992). parasites (Goh et al., 1999) or predators (The´odor, 1967; Many specimens of E. dabneyi hosting Pedicularia on their Robertson, 1970; Cate, 1973; Morton, 1988; Wu et al., 1990; branches have been collected in the Azores. The main goal of Goh and Chou, 1994; Oliverio et al., 1995; Schiaparelli et al., this study was to contribute to our knowledge of the association 2005). It is sometimes difficult to distinguish between parasitism between pediculariids and stylasterids, because most of the avail- and predation, so their functional classification remains uncertain able records of Pedicularia consist of empty shells or dead (Buhl-Mortensen and Mortensen, 2004). animals in mixed debris (Goud and Hoeksema, 2001), lacking The association between pediculariids and stylasterids has been any reference to the host species. Specific aims were: (i) to identify reported in 12 host species and one subspecies from several locations the Pedicularia individuals present in E. dabneyi colonies, and in the Atlantic and the Mediterranean (Table 1), with western describe shell morphology at various growth stages; (ii) to charac- Atlantic records rarer than those from the Northeast Atlantic and terize the Pedicularia traces found on the host; and (iii) to provide Mediterranean (Zibrowius and Cairns, 1992). Records for the new insights on the nature of this symbiotic relationship. The epi- Azores were mostly based on traces and identification to species fauna present on E. dabneyi is also briefly described. level was never achieved (Cairns, 1991; Zibrowius and Cairns, 1992), except a few observations made by Wisshak et al.(2009); Material and methods however, no method of identification was provided. Collection and examination of specimens Of the nine stylasterid species recorded for the Azores In situ observations of E. dabneyi hosting Pedicularia were made (reviewed by Zibrowius and Cairns, 1992), Errina dabneyi with the manned submersible “Lula” from the Rebicoff-Niggeler (Pourtale`s, 1871) is by far the most common. Unlike most Foundation. The dive was carried out on the southern slope # 2010 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved. For Permissions, please email: [email protected] 400 A. Braga-Henriques et al. Table 1. Pedicularia and their stylasterid hosts known for the Atlantic and the Mediterranean. Depth range Symbiont Host Locality (m) Reference One specimen + traces Errina atlantica Hickson, 1912 Azores 810–983 Zibrowius and Cairns (1992) One specimen + traces Errina dabneyi Pourtale`s, 1871 Azores 215–560 Zibrowius and Cairns (1992) Traces only Lepidopora eburnea Calvet, 1903 Azores 480–895 Zibrowius and Cairns (1992) P. sicula Swainson, 1840 Errina dabneyi Pourtale`s, 1871 Southern Faial Channel, 475; 490 Wisshak et al. (2009) Azores P. splendida Lorenz, 2008 Errina atlantica Hickson, 1912 Hye`res and Atlantis 845–1520 Lorenz (2008) Seamounts Downloaded from https://academic.oup.com/icesjms/article/68/2/399/614681 by guest on 23 September 2021 Traces only Stenohelia maderensis Johnson, 1862 Madeira 300–340 Zibrowius and Cairns (1992) Traces only Stylaster erubescens Pourtale`s, 1868 Blake Plateau, W Atlantic 505 Zibrowius and Cairns (1992) Traces only Stylaster complanatus Pourtale`s, 1867 Cuba, W Atlantic – Zibrowius and Cairns (1992) Traces only Crypthelia peircei Pourtale`s, 1867 Guadaloupe and St Vincent, – Zibrowius and Cairns W Atlantic (1992) Traces only Conopora sp. NW Brazil, W Atlantic – Zibrowius and Cairns (1992) P. tibia Simone, 2005 Stylaster sp. Canopus Bank, Brazil, W 60 Simone (2005) Atlantic P. bonfigliolii Cossignani, Stylaster sp. Canopus Bank, Brazil, W 60 Cossignani (2006) 2006a Atlantic P. sicula Swainson, 1840b Stylaster ibericus Zibrowius and Cairns, Bay of Biscay 500; 515 Zibrowius and Cairns 1992 (1992) Traces only Pliobothrus symmetricus Pourtale`s, 1868 Celtic Sea 380; 1050 Zibrowius and Cairns (1992) Traces only Stylaster erubescens britannicus Zibrowius Celtic Sea 1080 Zibrowius and Cairns and Cairns, 1992 (1992) P. sicula Swainson, 1840 Errina aspera Linnaeus, 1767 Strait of Gibraltar 61–443 A´lvarez-Pe´rez et al. (2005) P. sicula Swainson, 1840 Errina aspera Linnaeus, 1767 Mediterranean Sea about 100 Arnaud and Zibrowius (1979) P. sicula Swainson, 1840 Errina aspera Linnaeus, 1767 Mediterranean Sea 181–236 di Natale and Mangano (1985) P. sicula Swainson, 1840b Errina aspera Linnaeus, 1767 Mediterranean Sea 220–633 Zibrowius and Cairns (1992) P. sicula Swainson, 1840 Errina aspera Linnaeus, 1767 Strait of Messina, Sicily 100–300 + Giudice (1990) aPedicularia bonfigliolii was recently synonymized with the western Atlantic species Pedicularia decussata (Gould, 1855; see Lorenz and Fehse, 2009). bIdentity of Pedicularia sicula (and its synonymy) is given or confirmed by Bouchet and Ware´n (1993). of the Faial-Pico Channel (start position 38829′260′′N Pedicularia tibia Simone, 2005]. The species P. tibia and 28837′310′′W; end position 38829′400′′N28837′260′′W) between Pedicularia bonfigliolii Cossignani, 2006, both described from the depths of 330 and 480 m, on 4 September 2008. Specimens used same type of locality (Canopus Bank, Brazil), were treated by for detailed examination and measurement were obtained as Lorenz and Fehse (2009) as synonyms of P. decussata. This classi- bycatch from longline fishing cruises with RV “Arquipe´lago” fication is accepted for P. bonfigliolii, but is still controversial for P. (ARQDAC¸ O-03-P95; ARQDAC¸ O-29-P08) and from the local tibia (L. Simone, pers. comm.). Therefore, the latter species was longline fleet. A total of 43 living colonies of E. dabneyi have considered as a valid species. been collected over the past 14 years within the Azores EEZ, Some of the preserved specimens were soaked in distilled water from depths between 201 and 1097 m (Figure 1). The material is for 48 h without their shells for observation of anatomical charac- deposited in the collection of the Department of Oceanography ters. Finally, 10 squashes of Pedicularia stomachs were examined and Fisheries of the University of the Azores (DOP-UAz). under a light microscope to look for the presence of nematocysts Each colony was carefully examined