Population Characteristics, Habitat and Diet of a Recently Discovered Stingray Dasyatis Marianae: Implications for Conservation
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Journal of Fish Biology (2015) 86, 527–543 doi:10.1111/jfb.12572, available online at wileyonlinelibrary.com Population characteristics, habitat and diet of a recently discovered stingray Dasyatis marianae: implications for conservation T. L. A. Costa*†,J.A.Thayer*‡ and L. F. Mendes* *Ocean Laboratory, Department of Botany, Ecology and Zoology, Federal University of Rio Grande do Norte (UFRN), Campus Universitário, BR 101s/n Lagoa Nova, CEP 59072-970, Natal, RN, Brazil and ‡Farallon Institute for Advanced Ecosystem Research, 101 H Street, Suite Q, Petaluma, CA 94952, U.S.A. (Received 30 April 2014, Accepted 2 October 2014) This study examined population density, habitat and diet of Dasyatis marianae, a recently discovered species, in the reef complex of Maracajaú in Rio Grande do Norte state, Brazil. The highest concentra- tion of D. marianae occurred in seagrass beds. Habitat use differed significantly between sex and age classes, with females and juveniles using areas other than reefs. Females utilized primarily seagrass beds and juveniles occurred mainly along the sandy bottom near the beach, highlighting the importance of protecting these areas. Dasyatis marianae diet was characterized primarily by crustaceans (91⋅9% index of relative importance, IRI), including shrimp, crabs and lobsters. The availability of prey in different habitat types influences occupation by D. marianae, but the prey selectivity of D. marianae, among other factors, may affect this relationship. Intense shrimp and lobster fishing in the region prob- ably has an effect on preferred prey resources of this ray. Information on feeding habits of this species contributes to a better understanding of trophic dynamics and food webs, which is critical if ecosystem principles are to be integrated into fisheries management. © 2015 The Fisheries Society of the British Isles Key words: Brazil; elasmobranch; feeding habits; habitat use; population density; seagrass. INTRODUCTION The Brazilian large-eyed stingray Dasyatis marianae Gomes, Rosa & Gadig 2000 is registered as data-deficient on the IUCN red list due to the current level of information on its biology and life history (Rosa & Furtado, 2004). This stingray is endemic to Brazil with a distribution believed to be limited to the area between the north-east state of Maranhão and southern Bahia, although more sampling could possibly reveal a wider distribution (Rosa & Furtado, 2004). Dasyatis marianae occurs in a number of established marine protected areas (MPA), but is taken in small numbers in artisanal fisheries as by-catch where it is retained for consumption. It has also been reported in the ornamental fish trade in Bahia State (Rosa & Furtado, 2004). The few studies that exist suggest extensive spatial and temporal overlap of nursery areas among most †Author to whom correspondence should be addressed. Tel.: +55 084 99628169; email: tiegobiomar @gmail.com 527 © 2015 The Fisheries Society of the British Isles 528 T. L. A. COSTA ET AL. ray species in north-east Brazil with the exception of D. marianae (Yokota & Lessa, 2006), which may have a separate ecological niche and complicate conservation efforts. Further threats exist from indirect effects on coral-reef systems, such as sedimentation from deforestation and non-sustainable agricultural practices, coastal eutrophication and ocean temperature warming (Maida & Ferreira, 1997; Castro & Pires, 2001; Leão et al., 2003). Most elasmobranchs are K-selected, showing closely related recruitment and parental stock, and therefore survival during the juvenile phase is important for population stability (Stevens et al., 2000; Yokota & Lessa, 2006). This highlights the need for identification and protection of nursery areas as an important management and conser- vation strategy. Effective conservation requires knowledge of the spatial distribution of a species. Within certain geographic limits, individuals occupy habitats with adequate characteristics and their abundance depends directly on the availability of resources and presence of predators (Ricklefs, 1996). As rays are an abundant and species-rich group, their roles in the food webs of dem- ersal marine communities are probably very influential, although still relatively poorly understood (Ebert & Bizzarro, 2007). Some ray species are considered top predators (Macpherson & Roel, 1987; Ebert et al., 1991; Link et al., 2002; Orlov, 2003) and oth- ers are probably mid-trophic level predators (Myers et al., 2007; Ritchie & Johnson, 2009; Ajemian et al., 2012). Jacobsen & Bennett (2013) provide an overview of the dietary information available for stingrays (Suborder: Myliobatoidei) and electric rays (Suborder: Torpedinoidei) and show the trophic levels of stingrays, electric rays, skates and sharks from other studies. The same study also reveals that there are few studies on the diet of Myliobatoidei and Torpedinoidei rays compared with the number of studies of sharks and skates (Compagno, 1984). In general, elasmobranchs are important marine predators influencing lower trophic level fishes and invertebrate populations (Ellis et al., 1996; Cortés, 1999; Ebert & Biz- zarro, 2007). Yet despite their role in maintaining equilibrium and health of marine systems, there is still much to be understood about elasmobranch demography and ecology (Myers et al., 2007). This study focused on the feeding ecology and spatial distribution and population characteristics of D. marianae in the reef complex of Maracajaú, within an MPA, the coral-reef protected area (Área de Proteção Ambiental dos Recifes de Coral, APARC), in Rio Grande do Norte state. Specific habitat types were investigated where these fish are concentrated, their diet and trophic level characterized, and differences were quan- tified between sexes and stages of maturation. The diet was compared with indicesof prey availability developed from small-scale sampling in different habitats. Informa- tion on feeding habits contributes to a better understanding of trophic dynamics and food webs, which is critical if ecosystem principles are to be integrated into fisheries management and conservation. MATERIALS AND METHODS STUDY AREA The Maracajaú reef ecosystem (5∘ 21′ 12′′ S–5∘ 25′ 30′′ S; 35∘ 14′ 30′′ W–35∘ 17′ 12′′ W) is located off Rio Grande do Norte state, in north-eastern Brazil (Fig. 1). The reef complex covers c.10km× 4 km and is located 7 km offshore from Maracajaú beach (Mayal et al., 2009). © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 527–543 OCCUPATION PATTERNS AND DIET OF D. MARIANAE 529 ' 35° 30 35° 10' ' 05° 00 RN N Cioba Reef Zumbi Reef Touros Rio do Fogo Reef Rio do Fogo Sandy bottom near the beach Maracajaú Maracajaú Maracajaú Reef 0 km 4 010km ' B. Maxaranguape 05° 30 Fig. 1. Location of the Maracajaú coral-reef protected area (APARC, ) within Rio Grande do Norte state in north-eastern Brazil, highlighting the different study areas: , seagrass beds; , patch reefs; , sandy bottom near the reefs; , deeper area past the reefs; , unidentified; sandy bottom near the beach. Most of the reef base is composed of fossilized calcareous algae, corals and vermetids over a sandstone base which is exposed during low tides (Maida & Ferreira, 1997). Patches of reefs are interspersed with sandy or gravel bottom, and the complex also encompasses areas of seagrass [Halodule wrightii; Mayal et al. (2009)]. Water turbidity is generally high at high tide, although high visibility predominates between October and March. Water temperatures vary throughout the year from 22 to 27∘ C (Maida & Ferreira, 1997). The Maracajaú APARC was established in 2001 to regulate fishing and intense underwater tourism in the southern part of the reefs (Mayal et al., 2009). This MPA has been built on integrated participative management, supported by research and monitoring data. The five study areas consisted of (1) patch reefs (PR), (2) seagrass beds (SEB), (3) sandy bottom near the reefs (SBR), (4) a deeper area past the reefs with sand and gravel substrata (DPR) and (5) sandy bottom near the beach (SBB), which divided the reef complex according to the type of substratum (Fig. 1). POPULATION DENSITY To estimate D. marianae population density, visual censuses were conducted between July 2008 and July 2009 using the line-transect method (Helfman, 1992; Rosa & Moura, 1997). Each transect was 100 m long × 4 m wide and the number of individuals were counted in each transect. Counts were not possible along the sandy bottom near the beach (SBB) due to low visibility. All transects were geo-referenced (start and end points) with GPS and plotted according to the complex sub-area. Density in each sub-area was estimated, considering the number of D. marianae sighted on transects and the total area was sampled, assuming that the number of individuals in 1 km2 was proportional to the number of individuals recorded along the transect within that area. SAMPLE COLLECTION AND IDENTIFICATION Samples were taken from landings of the artisanal fleet at Maracajaú beach from August 2008 to August 2009 (with the exception of September, April and June). Dasyatis marianae was caught by gillnets, beach trawls, handlines and spearfishing. The fleet is composed of small motorized or sailing boats, and fishing occurs mainly between the beach and 25 km offshore, in depths between 1 and 30 m. Line fishing was conducted all year, while manual capture was used mainly during December to March. © 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 527–543