INTRODUCTION
The king helmet Cassis tuberosa (Linnaeus, 1758) is one of the most exploited large marine gastropods of the Brazilian coast for use as marine curios, traditional medicines and for magic-religious purposes (Alves & Dias, Reference Alves and Dias2010; Dias et al., Reference Dias, Léo-Neto and Alves2011). It inhabits shallow back reef habitats and sandy shores, but it can also be found in depths from 1 to 10 m (Rios, Reference Rios2009). According to Rios (Reference Rios2009), it occurs from North Carolina to Brazil. Rios (Reference Rios2009) and Rolán (Reference Rolán2005) also recorded C. tuberosa in Cape Verde, western Africa. In Brazil, it is distributed from the state of Maranhão to south Bahia, including the Fernando de Noronha and Abrolhos archipelagos (Rios, Reference Rios2009).
As a specialist predator that feeds exclusively on echinoids, mainly sea urchins (Hughes & Hughes, Reference Hughes and Hughes1981), C. tuberosa plays a key ecological role in marine environments. The predation of C. tuberosa on sea urchins is important to control the populations of these herbivores, thus limiting the macroalgal overgrowth and favouring the recruitment of coral larvae to reef habitats (Mumby et al., Reference Mumby, Harborne, Williams, Kappel, Brumbaugh, Micheli, Holmes, Dahlgren, Paris and Blackwell2007). Despite its ecological relevance, information on the biology and ecology of this species is scarce.
In this study, we provide the first record of C. tuberosa spawning in the wild, as well as a description of the behaviour performed for this activity and characteristics of the microhabitat used to release the eggs. Although in low density, adults are often observed in coastal habitats on the north-east coast of Brazil; however, recruits and juveniles of this species are rarely found. In this sense, this record of spawning is the first step towards understanding the reproductive needs of this species, which is currently a target of the international shell trade.
MATERIALS AND METHODS
The spawning behaviour of the specimen was observed in December 2013 in the protected reefs of Tamandaré (8°45′46″S 35°05′33″W), a reef formation belonging to the Costa dos Corais Environmental Protection Area (CCEPA), state of Pernambuco, north-eastern Brazil (Figure 1). CCEPA is the largest marine protected area in Brazil (total area: 404,279.93 hectares) and includes no-take zones with permanent monitoring. In the adjacent areas, fishing and tourism activities are frequent. The reef environment is very close to the beach and combines a mosaic of underwater biotopes such as coral reefs, seagrass beds, macroalgae banks, coral rubble and sand bottoms.
(A) Location of Costa dos Corais Environmental Protection Area (CCEPA) along the coast of Pernambuco State, north-eastern Brazil; (B) Location of Tamandaré reefs with indication (
) of the site of spawning (illustration © Ellori Mota).
The shell length of the specimen was measured in cm by using a millimetre tape. The following data were also obtained in situ: temperature and depth in the spawning site, microhabitat used for laying eggs, colour, size and general characteristics of spawning (e.g. number, height, shape and distance among egg capsules). The microhabitat characteristics of Cassis tuberosa were also recorded.
RESULTS AND DISCUSSION
One adult individual (19 cm in shell length) of Cassis tuberosa was observed releasing egg mass at 11:00–12:00 a.m. on an algal turf of the foliose macroalgae genus Padina (Figure 2A). The specimen was laying over gravel substrate surrounded by macroalgae at a depth of 2 m (Figure 2A, B). The oothecae were arranged in a single layer measuring 13 × 10 cm (width × length). The egg mass consisted of approximately 200 vasiform capsules, orange in colour (Figure 2C, D). Their peduncles were 1.5 cm in height and set 2–3 mm apart. In apical view, capsules are quadrangular. Spawning lasted for at least 2 h, and after laying the egg mass, Cassis tuberosa moved 0.5 m out of the algae-substrate and partially buried itself (Figure 2E).
(A) Adult Cassis tuberosa over the algal turf, at a depth of 2 m, in the Costa dos Corais Environmental Protection Area (north-east Brazil); (B, C) Detail of the king helmet releasing the egg mass; (D) Spawning of C. tuberosa on the fronds of Padina sp.; (E) Cassis tuberosa separate from the algal turf after laying the egg mass (photographs © Thelma Dias).
While the king helmet was still spawning, the reef fish Halichoeres poeyi (Steindachner, 1867) carried out three consecutive attacks on the egg mass. When Cassis tuberosa left the substrate of spawning, the algal turf took a position that completely hid the oothecae, leaving it protected between the fronds. Despite the occurrence of large adults in several coastal areas, spawning of Cassis tuberosa has never been described or recorded in the wild.
According to D'Asaro (Reference D'Asaro1963), there is a great variability in the spawning of the Cassidae; however, the spawn of Cassis tuberosa is quite similar to that produced by its congener, Cassis madagascariensis Lamarck, 1822. Nevertheless, Cassis madagascariensis utilizes coarse, carbonate sand to spawn (D'Asaro, Reference D'Asaro1963; Lindsey & Gerace, Reference Lindsay and Gerace1994), while Cassis tuberosa spawns in the algal fronds.
The main component of the microhabitat of Cassis tuberosa, i.e. macroalgal banks, seems to play a key role in serving as substrate for egg mass deposition by this species. Detecting the essential fish habitat is an important tool to ensure the conservation of exploited populations (Glazer & Kidney, Reference Glazer and Kidney2004), and to develop management strategies that promote the increase of biomass and abundance of the target species. Since the CCEPA is a priority area for marine conservation in Brazil, management initiatives should include the protection of algal beds.
Therefore, protecting the population stocks of target species would ensure that the ecological role developed by this species is successfully performed. This inedited record of Cassis tuberosa spawning could, in addition to expanding our knowledge of the biology of this species, contribute to assessing the effectiveness of the largest marine protected area in protecting exploited species, ensuring the development of reproductively active individuals.
ACKNOWLEDGEMENTS
The PADI Foundation (grant no. 8069) and Conchologists of America (2013 Grants to Malacology) provided financial support and Prof Mauro Maida of the Instituto Recifes Costeiros provided logistical support. The study was authorized by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio – license no. 35487-2). We are grateful to Luis Carlos for his essential support in the field. Two reviewers improved the text.
