Population Characteristics, Habitat and Diet of a Recently Discovered Stingray Dasyatis Marianae: Implications for Conservation

Home , Blue stingray, Golden cownose ray, Panulirus echinatus, Spotted eagle ray

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 concentration 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 probably 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

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 conservation 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 demersal 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).

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.

Specimens were identified based on Gomes et al. (2000). They were aged using size (disc width, WD), and sizes at sexual maturity were estimated by macroscopic evaluation according to Snelson et al. (1988) and Smith et al. (2007).

DIET CHARACTERIZATION Prey were identified to the lowest possible taxon. Stomach contents identified as baitwere excluded from analyses (relatively large pieces of fishes or shrimp with straight edges, indicating the use of cutting tools). The cumulative numbers of randomly pooled stomach samples were plotted against the cumulative number of prey groups identified to determine the minimum number of stomachs required for adequate description of the diet (Cortés, 1997). To ensure that curves reached an asymptotic value, 10 random orders of stomachs (curves) were calculated (Koen-Alonso et al., 2002). The contribution of each prey taxon to D. marianae diet was expressed as per cent frequency of occurrence (%FO), number percentage (%N) and mass percentage (%W). Empty stomachs (n = 1) were not considered in the estimates of %FO. As these prey indices provide different insights into feeding habits (Link, 2004), an integrated index, the index of relative importance [IRI = % FO(% N + % W)] (Pinkas et al., 1971) expressed as a percentage (Cortés, 1997), was calculated. ( ) ∑n Trophic levels (TL) were calculated using the following equation: TLk = 1 + j=1 pjTLj , where TLk is the trophic level of species k, pj is proportion of prey category j in the diet of species k, n is total number of prey categories and TLj is the trophic level of prey category j (Cortés, 1999). The TL of prey categories was taken from sources within Ebert & Bizzarro (2007) and Jacobsen & Bennett (2013) who calculated trophic levels of many skate and ray species. The trophic level of D. marianae was then compared with the results of these authors. The categories of preference of food items were defined using the method of the feed coefficient (Q; Hureau, 1970), obtained by: Q = (W %)(N %). According to this method, the examined item is considered a preferred prey when Q ≥ 200, secondary prey when 20 < Q < 200 and occasional when Q ≤ 20. The four substratum types where D. marianae were caught (PR, SEB, DPR and SBB) were sampled to create indices of prey availability against which to compare diet. Each area was divided into three parts and one point was chosen randomly within each part and recorded using GPS. Each point was sampled three times over a span of 4 months (October 2010 to January 2011) using a 3 mm mesh net attached to a small, modified Surber sampler (30 cm × 30 cm) with a solid metal bottom. Transects were created to mimic the observed feeding habits of D. marianae. The trawl was guided by a diver and pulled along the benthos by a small outboard boat for c. 30 m for each sample, to collect demersal prey both on the surface and buried up to several cm in the substratum. Contents of each net were immediately poured into sample bags and stored in 70% isopropyl alcohol. Prey were separated from substrata in the laboratory and identified to the lowest possible taxon.

ANALYSES Chi-squared paired tests were used to compare areas of capture for habitat characterization between male and female D. marianae, and between juveniles and adults. Analysis of multinomial proportion (Goodman, 1964) was used to examine the distribution of adults among areas. To examine whether prey availability was a driving factor in the distribution of D. marianae, diet composition was compared with the index of prey availability from small-scale trawls during October to January. Multidimensional scaling (MDS), multivariate analysis of variance (ANOVA; ANOSIM) and similarity percentage analysis (SIMPER) in the PRIMER-E statistics 6.1.5 (Primer-E Ltd; www.primer-e.com) were used to graphically represent and quantitatively compare diet among habitats and among D. marianae and indices of prey availability. Prey species or groupings were included in these analyses if they contributed to 95% of D. marianae diet as measured by ranked cumulative %FO. Data were not transformed because they were already weighted by dominant taxa. MDS plots were based on triangular matrices of Bray–Curtis similarities of the IRI for each prey species. Stress values were calculated to give

Table I. Density estimates from visual surveys of Dasyatis marianae in the Maracajaú reefs region (see Fig. 1)

Substratum type PR DPR SEB SBR Overall Number of transects 57 50 56 50 213 Sampled area (km2)0⋅023 0⋅020 0⋅022 0⋅020 0⋅085 Number of D. marianae 2 (males) 6 21 1 30 observed (4 males; (6 males; (male) (13 males; 2 females) 15 females) 17 females) Frequency (%) 1⋅810⋅028⋅62⋅010⋅8 Population density (number 88 300 938 50 352 individuals km−2)

PR, patch reefs; DPR, deeper area past the reefs; SEB, seagrass beds; SBR, sandy bottom near the reefs. an indication if and to what extent data were distorted (or scattered). Stress values < 0⋅10 were regarded as being unlikely to result in misinterpretation of the data (Clarke & Warwick, 2001).

RESULTS

POPULATION CHARACTERISTICS A total of 30 individuals of D. marianae were observed on surveys of 213 transects covering each of the four habitat types. Overall density of D. marianae was 352 individuals km−2 (mean density ± S.D. = 344 ± 411, in the sampled areas). The highest concentration of individuals was recorded in the seagrass beds, with 938 individuals km−2 and the lowest concentration along the sandy bottom near the reefs at 50 individuals km−2 (Table I). The difference in the number of males and females per area 𝜒2 ⋅ was significant only for SEB, with more females in this area( SEB = 3 9, d.f. = 1, < ⋅ 𝜒2 ⋅ > ⋅ 𝜒2 ⋅ > ⋅ 𝜒2 ⋅ P 0 05; PR = 2 0, d.f. = 1, P 0 05; SBR = 1 0, d.f. = 1, P 0 05; DPR = 0 7, d.f. = 1, P > 0⋅05). A total of 120 D. marianae were sampled from the artisanal fishing catch, con- sisting of 36 adult females (measuring between 27–33 cm WD and 870–1860 g), 71 adult males (24–28 cm WD and 500–900 g) and 13 immatures (14–24 cm WD and 84–610 g). Visual assessment of the stage of maturation suggested that maturity for males and females occurred at 24 and 27 cm WD, respectively. Of the females, 25% were gravid (n = 8; between 27–32 cm WD and 970–1580 g). Catches were distributed as follows: sandy bottom near the beach (n = 24), seagrass beds (30), patch reefs (24), deeper area past the reefs (32), unidentified areas (10). Excluding unknown areas from analysis, sex differences among habitats in which 𝜒2 ⋅ < ⋅ D. marianae were captured were significant ( sex = 8 2, d.f. = 1, P 0 01; Table II). 𝜒2 ⋅ Males were found more often in the reefs and outlying areas ( PR = 10 7, d.f. = 1, < ⋅ 𝜒2 ⋅ < ⋅ P 0 001; DPR = 6 1, d.f. = 1, P 0 01), while females primarily used the seagrass 𝜒2 ⋅ beds although the sex ratio difference was not significant within this area ( SEB = 0 1, d.f. = 1, P > 0⋅05). There was no sex ratio difference in the sandy bottom near the 𝜒2 ⋅ > ⋅ beach ( SBB = 0 2, d.f. = 1, P 0 05). There was, however, a highly significant stage 𝜒2 ⋅ < ⋅ difference between this and other areas ( immature = 19 1, d.f. = 3, P 0 001), with immatures concentrated near the beach and adults further offshore.

Table II. Sex and age differences among habitats in which Dasyatis marianae was captured in Maracajaú reefs region (see Fig. 1)

𝜒2 𝜒2 Habitat types n Male Female sex P Immature Adult* age P ⋅ > ⋅ ⋅ > ⋅ SBB 24 13 11 0 2 0 05 11 13bc 0 2 0 05 ⋅ > ⋅ ⋅ < ⋅ SEB 30 14 16 0 1 0 05 1 29ac 26 1 0 001 ⋅ < ⋅ ⋅ < ⋅ PR 24 20 4 10 7 0 001 0 24ab 24 0 0 001 ⋅ < ⋅ ⋅ < ⋅ DPR 32 23 9 6 1 0 01 0 32a 32 0 0 001 Total 110 70 40 8⋅2 <0⋅01 12 98 67⋅2 < 0⋅001

PR, patch reefs; DPR, deeper area past the reefs; SEB, seagrass beds; SBR, sandy bottom near the reefs. *Different lower-case letters represent statistical differences (P < 0⋅05) of adult distribution among areas.

PREY UTILIZATION Of the 120 specimens collected, 101 stomachs were analysed. Cumulative prey curves showed that a minimum of c. 37 samples were required to represent main prey (those contributing to 95% of diet by ranked cumulative %FO). Diet of D. marianae was represented by five phyla (Arthropoda, Sipuncula, Echinodermata, Anelida and Nematoda; Table III). Primary prey was comprised of arthropod crustaceans, specifically crabs (Infraorder Brachyura) and prawns (Suborder Dendrobranchi- ata), and also consisted of mantis shrimps (Order Stomatopoda), isopods (Order Isopoda) and spiny lobsters (Family Palinuridae), with trace amounts of hermit crabs (Infraorder Anomura), burrowing shrimps (Infraorder Thalassinidea), and small benthic crustaceans of the Order Tanaidacea. The trophic level of D. marianae was 3⋅6. This was lower than that of many other similar taxonomic groups (Table IV). A MDS plot of prey availability in the environment v. diet composition revealed only partial overlap (Fig. 2). A stress value of 0⋅18 for the two-dimensional plot indicated that this was not a satisfactory representation of the diet composition v. prey availability data; a three-dimensional configuration improved the fit (stress = 0⋅12; Fig. 2), but still did not succeed in reducing the stress value below the recommended level of 0⋅10. In terms of prey availability, polychaetes were the most common prey sampled, with the highest concentration along the sandy bottom near the beach. The most important diet type, crustaceans, was found primarily in the seagrass beds, although the sandy bottom near the beach also contained prawns (Table V). Crabs were the most important diet item for adults, in particular for adult females, found mostly in seagrass beds. Immatures, which were found primarily on sandy bottom near the beach, relied most heavily on prawns. Lobster was found in the stomachs of adult females in all habitats in which they were captured, albeit in low percentages. Trawls were significantly different from overall D. marianae diet composition from August to August (ANOSIM, r2 = 0⋅79, P < 0⋅01; Table VI), as well as from Octo- ber to January (r2 = 0⋅81, P < 0⋅01). There was no lobster sampled in the environment, despite the fact that it showed up in the diet (Table VI). Conversely, amphipods, molluscs and small benthic fishes (Uranoscopidae and Gobiesocidae) were sampled inthe environment, but did not occur in the diet. Levels of hermit crabs were higher in the environment than in the diet. Of all areas, seagrass beds were the most similar between diet and environment, both containing a high percentage of crabs and prawns, the most important prey of D. marianae.

© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 527–543 OCCUPATION PATTERNS AND DIET OF D. MARIANAE 533 Q 0OP 0OP 2SP 0PP 9PP 00 OP 2OP 9SP 0OP 4OP ⋅ ⋅ RI 8SP 2OP 4OP ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ I ) Q 83 612 00 82 629 91 534 00 00 614 81 ), mass percentage %% 90 00 ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ O N 340 01 618 239 99 448 11 21 741 015 721 16 75 ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ WF ⋅ ⋅ ⋅ % 17 511 60 03 20 14 114 14 935 32 20 314 61 ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ ⋅ N 5 1 ) and feed coefficient ( RI I ), the integrated index of relative occurrence (% O F diet between August 2008 and August 2009, shown as number percentage (% Dasyatis marianae ), per cent frequency of occurrence (% W (% Table III. Prey taxa identified in PhylumSipuncula Subphylum Class OrderArthropoda Suborder CrustaceaPP, preferred prey; SP, Infraorder secondary.prey; OP, occasional prey. Malacostraca Family Tanaidacea % 0 Anelida Polychaeta 10 Arthropoda Crustacea Unidentified 5 Nematoda Echinodermata Holothuroidea 1 Arthropoda Crustacea Malacostraca Decapoda Dendrobranchiata 39 Arthropoda Crustacea Malacostraca Decapoda Pleocyemata Palinura Palinuridae 2 Arthropoda Crustacea Malacostraca Decapoda Pleocyemata Brachyura 16 Arthropoda Crustacea Malacostraca Decapoda Pleocyemata Thalassinidea 1 Arthropoda Crustacea Malacostraca Decapoda Pleocyemata Anomura 0 Arthropoda Crustacea Malacostraca Stomatopoda 11 Arthropoda Crustacea Malacostraca Isopoda 5

Table IV. Trophic level (TL)ofDasyatis marianae compared with other rays

Taxon n Mean TL Source D. marianae (Dasyatidae) 101 3⋅6 This study Dasyatidae 6515 3⋅62 Jacobsen and Bennett (2013) Urotrygonidae 1812 3⋅52 Jacobsen & Bennett (2013) Narcinidae 630 3⋅66 Jacobsen & Bennett (2013) Urolophidae 1166 3⋅70 Jacobsen & Bennett (2013) Potamotrygonidae 470 3⋅71 Jacobsen & Bennett (2013) Gymnuridae 942 4⋅16 Jacobsen & Bennett (2013) Anacanthobatidae 1 3⋅5 Ebert & Bizzarro (2007) Rajidae 40 3⋅8 Ebert & Bizzarro (2007) Arhynchobatidae 19 3⋅9 Ebert & Bizzarro (2007) n, total number of stomachs analysed.

DISCUSSION

POPULATION DENSITY The survey results showed a high mean density of D. marianae in the reef complex of Maracajaú (344 individuals km−2), although with a high margin of s.d. (±411). Extrapolating the surveys based on density per habitat type and approximate area cov- ered by each habitat in the Maracajaú reef region would result in a population estimate of 4225 individuals. The few other existing studies that used visual censuses for estimating density of Dasyatidae showed compatible results. In the Fernando de Noronha

Resemblance: S17 Bray–Curtis similarity 3D Stress: 0·12

Fig. 2. Multidimensional scaling (MDS) ordination of Dasyatis marianae diet composition ( ) based on a Bray–Curtis similarity index of measured as per cent index of relative importance, %IRI, v. prey availability surveys in the same area ( ), based on a Bray–Curtis similarity index of catch rates.

Table V. Mean diet composition (measured as per cent index of relative importance, %IRI) of Dasyatis marianae immatures, adult females and males in comparison with prey availability sampled in the environment (see Fig. 1) Habitat Brachyura Prawns (Caridea and Stomatopoda Isopoda Palinuridae Anomura Other Crustacea Echinodermata Polychaeta Sipuncula Dendrobranchiata)

Environment SBB 4⋅718⋅00⋅11⋅30 0⋅50 0 32⋅50⋅9 SEB 10⋅524⋅70⋅10 0 2⋅00 0⋅11⋅40 PR 1⋅11⋅50⋅10⋅20 0⋅30⋅10 9⋅70 DPR 0⋅80 0 0⋅10 0 0 0 2⋅20 Overall 4⋅89⋅3 <0⋅10⋅30 0⋅70 0 6⋅90⋅1 Immatures SBB 0⋅974⋅92⋅319⋅30 0 1⋅10 1⋅50 SEB 37⋅319⋅115⋅80 0 0 13⋅20 11⋅80 PR 27⋅023⋅513⋅65⋅00 0 5⋅40 4⋅520⋅9 DPR 17⋅29⋅514⋅39⋅70 0 0 0 0 49⋅3 Overall 4⋅274⋅73⋅813⋅10 0 1⋅70 1⋅40⋅9 Adult females SBB 82⋅60 3⋅50 3⋅60 2⋅90 7⋅30 SEB 45⋅17⋅111⋅30⋅15⋅60 6⋅62⋅216⋅53⋅9 PR 76⋅24⋅54⋅12⋅57⋅20 1⋅40 0 4⋅0 DPR 29⋅655⋅81⋅50⋅72⋅10 0⋅80 8⋅21⋅4 Overall 47⋅822⋅56⋅30⋅74⋅30 4⋅10⋅311⋅22⋅6 Adult males SBB 86⋅97⋅95⋅2000 00 0 0 SEB 4⋅510⋅261⋅51⋅60 0 0⋅20 17⋅93⋅7 PR 25⋅821⋅024⋅700⋅10⋅20⋅90⋅717⋅98⋅5 DPR 28⋅08⋅027⋅30⋅80⋅10 3⋅52⋅020⋅48⋅7 Overall 24⋅016⋅631⋅40⋅70⋅10 1⋅50⋅518⋅36⋅1

PR, patch reefs; DPR, deeper area past the reefs; SEB, seagrass beds; SBR, sandy bottom near the reefs.

Archipelago, Brazil, a mean ± s.d. density of 365 ± 424 individuals km−2 of southern stingray Dasyatis americana Hildebrand & Schroeder 1928 was measured (A. A. Aguiar, unpubl. data). Tilley & Strindberg (2013) estimated the density of D. americana at Glovers Reef Atoll, Belize, at 245 individuals km−2 and also extrapolated their survey results to estimate a population of c. 8400 individuals at that location. Estimates of population density of elasmobranchs through underwater visual census are not common and exhibit deviations inherent in the method. Most elasmobranchs are highly mobile and surveyed individuals may be recorded repeatedly and in different areas. Unfortunately, although the mark–recapture method would be preferable to avoid these pitfalls (Kohler & Turner, 2001; Castro & Rosa, 2005; Marshall et al., 2011), recaptures of this and similar species are often very low and do not provide adequate estimates. Furthermore, the resources were not available for such a survey and often recaptures are very low and do not give adequate estimates. Therefore, although

Table VI. Analysis of similarity (ANOSIM) test results of significantP ( ≤ 0⋅05) differences in Dasyatis marianae diet composition v. food availability in the environment (see Fig. 1). Prey contributing to significant diet differences (up to 90%) were identified by similarity percentage (SIMPER) analysis

SIMPER ANOSIM Phylum Arthropoda Brachyura Prawns (Dendrobranchiata Stomatopoda Amphipoda Anomura Isopoda Palinuridae Polychaeta Sipuncula Molusca Echinodermata Perciformes Mean dissimilarity Other Crustacea um

Global test & Caridea) Pair-wise r2 P tests 0⋅79 <0⋅01 SBB 0⋅24 >0⋅05 17⋅019⋅410⋅41⋅70⋅710⋅30⋅53⋅629⋅92⋅20⋅14⋅1081⋅0 SEB 0⋅02 >0⋅05 20⋅120⋅516⋅43⋅85⋅33⋅22⋅35⋅811⋅44⋅20⋅46⋅7072⋅3 PR 0⋅30 <0⋅01 16⋅57⋅411⋅53⋅06⋅61⋅21⋅79⋅523⋅45⋅97⋅42⋅53⋅485⋅6 DPR 0⋅41 <0⋅01 22⋅215⋅215⋅93⋅80 2⋅71⋅14⋅115⋅311⋅94⋅32⋅90⋅597⋅0

PR, patch reefs; DPR, deeper area past the reefs; SEB, seagrass beds; SBR, sandy bottom near the reefs.

specific population estimates using visual censuses are unreliable, the high occurrence of individuals in particular areas may indicate the importance of those areas, as in this study. Obtaining such data is very important to the management and conservation of local populations through habitat preservation.

IMPORTANCE OF NON-REEF HABITAT A high density of D. marianae was found in areas of seagrass beds and prey availability probably influences the local distribution, with crustaceans, mainly crabs and prawns, being most concentrated in this habitat. Seagrass beds appeared to be the preferred habitat of adult females, while immature fish were concentrated along the sandy bottom near the beach (Table II), reflecting the availability of their preferred prey taking the study area as a whole. Although productivity and juvenile survival are important for K-selected species, these areas show special importance for species conservation, instead of focus on the reef itself. Yokota & Lessa (2006) indicated that some ray species make use of coastal and turbid waters as nursery areas throughout the year, but did not relate the distribution of rays to seagrass beds. In this work, the importance of non-reef areas is demonstrated for D. marianae, a species initially described as associated with reefs (Gomes et al., 2000). Few conservation actions are aimed at non-reef areas, unlike reefs themselves. The sandy bottom near the beach is mainly affected by high accessibility and all the effects of uncontrolled coastal occupation, such as input of pollutants and sediment (Curran et al., 2002), and shrimp beach trawl fisheries. Locally, seagrass beds suffer

© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 527–543 OCCUPATION PATTERNS AND DIET OF D. MARIANAE 537 primarily from threats associated with purse-seine fishing of the halfbeak fishes (Hemiramphidae), fishing of octopus by diving and traditional fishing with hookand line. The seagrass beds are also feeding areas for other conservation targets, such as turtles and manatees (Valentine & Heck, 1999; Castelblanco-Martínez et al., 2009).

DIET SPECIALIZATION Dasyatis marianae is a specialist predator with a carcinophagic preference (Table III). A number of studies indicate crustaceans as important items in the diet of Dasyatidae (Navia et al., 2007; Lopez-Garcia et al., 2012; Jacobsen & Bennett, 2013), as found in this study. Some dasyatid species also feed on teleosts (Gilliam & Sullivan, 1993; Taniuchi & Shimizu, 1993; Ebert & Cowley, 2003). In all these studies, the authors suggest an opportunistic strategy where the most abundant prey are captured. These and other studies did not, however, evaluate the availability of prey in the species occurrence area, an aspect fundamental to understanding the feeding strategy used by these predators. In this study, however, a variety of molluscs, amphipods and fishes occurred in the habitats occupied by D. marianae, but these prey were not found in the diet. A teleost was observed in the stomach of a specimen of D. marianae from another region, Ceará, Brazil (T. L. A. Costa, unpubl. data), indicating that teleosts may be complementary or occasional prey for this species. Motta et al. (2009) also recorded the occurrence of bony fishes (two Scaridae) in the stomach of a very large female D. marianae (38 cm WD) at the Manoel Luís Reefs in Maranhão, Brazil. Local fishermen in Maracajaú also use bony fishes as bait to catch this species, further suggesting that D. marianae will also scavenge small dead or dying fishes. Lobster did not appear to be a primary prey (forming c. 10% of the diet), but adult female D. marianae were found with lobster in their stomachs in all habitats sampled. This was despite the fact that no lobster were sampled in trawl surveys, indicating that lobsters are sought after by adult females, even when in low abundance in the sampled areas (Table V). Sidwell et al. (1974) measured a higher energy value for lobsters (0⋅3975 kJ 100 g−1) compared with other prey of D. marianae (crab = 0⋅3410 kJ 100 g−1; shrimp = 0⋅3694 kJ 100 g−1). This indicates that lobster is probably a preferred prey and may contribute to female breeding condition, a period when more energy is required for the development of embryos. Dasyatis marianae captured in areas other than seagrass beds may be feeding (due to preference of prey types) and moving to other areas before food is digested, as digestion times in this species are unknown. This could explain the high levels of dissimilarity between diet and prey availability in the patch reefs, deeper areas past the reef, in adult males, and the sandy bottom near the beach in juveniles (Table VI). Young D. marianae, for example, are concentrated in the sandy bottom near the beach, where there is lower availability of prawns compared with the seagrass beds. Immatures may prefer more turbid and shallow waters (even with lower availability of their preferred prey) rather than an environment with more prey (seagrass beds), but deeper and more exposed, thus minimizing their vulnerability to predation. Yokota & Lessa (2006) explain that predation risk would be reduced through the limitation of juvenile rays to shallower, more turbid waters, and this study suggests that D. marianae may use coastal sandbanks as a primary nursery. According to Heupel et al. (2007), some species may trade low food availability for lower predation rates and the nursery areas may be more food limited than previously contended by studies in these areas.

Adult males occupied patch reefs and deeper areas past the reefs in higher frequen- cies (Table II). This may be explained as exploratory behaviour. Adult males are less vulnerable (larger than juveniles and without the need to sustain embryos) and thus may explore more exposed environments to obtain a larger variety of prey. Even while consuming more Polychaeta (prey with greater availability in the patch reefs and past the reefs) than immature and adult females, adult males are probably still searching for crustaceans, especially Stomatopoda (Table V). Crustaceans are prevalent in seagrass beds, but even in other areas D. marianae search for this important resource, contributing to the dissimilarity between diet and prey availability. Trophic level, which was also calculated in this study, can be important to help under- stand food web position, although there are many problems with this calculation. In addition to issues of standardization of trophic level sources for prey groups, other problems include ontogenetic diet differences of prey, overly broad prey categories used to calculate trophic level values (i.e. generalization of trophic level over large prey groups due to lack of more specific information on prey species or families), and regional differences [i.e. lack of trophic level information for prey groups in the south-west Atlantic Ocean where this study was conducted; Ebert & Bizzarro (2007); Jacobsen & Bennett (2013)]. These examples highlight the importance of calculating and perhaps refining prey categories that are more realistic to the predator in question (Ebert & Bizzarro, 2007). A good tool for further study may be the use of stable isotopes to calculate trophic levels of species, even by sex or maturity stage.

FISHING EFFECTS Lobsters of the family Palinuridae are considered the most important economic resource of the fishing industry in north-eastern Brazil (Pinheiro et al., 2003). They were exhausted dramatically in recent decades as a result of overfishing, including illegal fishing (Pinheiro & Lins-Oliveira, 2006; Barreto et al, 2009), but there are no data on targeted fishing for lobster in the study area. Lobsters are probably preferred, high-energy prey for D. marianae, and thus the reduction of this food source could have negative population consequences for D. marianae. Lobsters may in the past have played a more important role in the diet of D. marianae than was observed in this study, and may still be important in areas with more limited human exploitation of this resource. Many authors show that dietary changes occur when preferred prey decrease (Abrams & Ginzburg, 2000; Field et al., 2006). Trites et al. (2007) comment that a dietary shift to low energy prey may further exacerbate effects of decreased prey availability by increasing food requirements. In this case, adult female D. marianae that need to sustain embryos may need to feed more, when lobsters are not available. Prawns and crabs were the primary prey of D. marianae in the Maracajaú region (Table III). Artisanal fisheries with beach trawls target prawns, and crabs are caught as by-catch. Prawn fishing may have particularly strong implications for immature D. marianae as prawns comprise such a high percentage of their diet (Table V), and most immature fish were found near the beach (Table II). The removal of key prey species has direct effects on food webs and can be destabiliz- ing to ecological regimes (Osterblom et al., 2007; Baum & Worm, 2009). Fishing can exacerbate climate effects on fished populations (Hsieh et al., 2006; Anderson et al., 2008) and several studies show that after the disappearance of a primary prey, predators

© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 527–543 OCCUPATION PATTERNS AND DIET OF D. MARIANAE 539 exhibit a decrease in reproductive success and eventual reduction in their population size (Chiaradia et al., 2010). There is also fishing mortality of D. marianae, directly and indirectly (by-catch). Although not commercially exploited, it is occasionally caught for consumption in various locations along the north-east coast of Brazil. Although historically considered of low economic value, and seldom fished, several species of batoids have become the target of commercial fishing and their importance to fisheries has been increasing (Biz- zarro et al., 2007; Smith et al., 2008). This phenomenon may be occurring to replace catches of bony fishes whose stocks are declining (Rezende et al., 2003). Spatially concentrated capture effort may affect the resilience of this species, compromising the population in the medium and long term. The ease of capturing D. marianae in some localities, particularly due to concentrations around reef complexes and associated habitat, coupled with the decline of many stocks of other species, creates a dangerous setting and highlights the urgency to develop efficient management tools for this species.

CONSERVATION APPROACHES Fishing quotas and size class restrictions, for both D. marianae and important prey types (prawn, crab and lobster), would probably be beneficial, although agency and enforcement difficulties exist. Habitat protection may be a quicker and more effective tool, given the existing MPA at Maracajaú and in the north-east of the country (c.10 MPAs). Levin & Stunz (2005) explain that ecosystem-based management relies on the ability to efficiently assess critical habitat necessary for ecosystem sustainability. For fisheries, this is also known as essential fish habitat, and means those waters andsub- strata necessary to fish for their spawning, breeding, feeding and growth to maturity (Department of Commerce, 1997). Thus, the identification of areas that support these sensitive life stages and areas where high densities of organisms at critical life stages occur is the logical first step for prioritizing certain areas for conservation andman- agement (Levin & Stunz, 2005; Kinney & Simpfendorfer, 2009). One approach is the protection of juvenile nursery grounds (sandy bottom near the beach) and areas where gravid females feed (seagrass beds), potentially through limiting fishing in certain areas (spatial restriction) or during certain months (temporal restriction), protecting the final stage of gestation or another stage. Ecotourism should not be overlooked as a tool. Observation of and education about elasmobranchs is important because it can lead to greater awareness and support for conservation (Garrod & Wilson, 2003). Well-managed ecotourism sites usually have resulted in improved health and ecosystem structure (Cisneros-Montemayor et al., 2013). Elasmobranchs occur in all oceans of the world, but few species are accessible to tourists in areas that exploit the observation of these animals (Gallagher & Hammerschlag, 2011; Cisneros-Montemayor et al., 2013). In the APARC, diving conditions and access to viewing of species such as D. marianae may financially benefit this and other MPAs and support effective conservation. Perhaps, the most effective vehicle for education and outreach is community mem- bers themselves. This is particularly important for the artisanal fisheries conducted by diving and visual capture in the seagrass beds along the north-east coast of Brazil. Education on the importance of throwing back small individuals that are probably immature (<23 cm), or gravid females, primarily in the beach-seine fishery, could aid

© 2015 The Fisheries Society of the British Isles, Journal of Fish Biology 2015, 86, 527–543 540 T. L. A. COSTA ET AL. in increasing breeding success and recruitment to the population. Finally, outreach on the community role and ecosystem services provided by D. marianae (the role they play in the food web and stability of the reef ecosystem) is important for public appre- ciation of sustainability for future generations of fishers and tourists for the continued economic viability of Maracajaú and other similar communities.

We would like to thank the fishers of Maracajaú, without whose help this project would not have been possible; The Fulbright International Scholar Programme which supported J.A.T.’s stay at UFRN for the completion of this work; R. F. Amarral for providing the original image representation of the reef complex of the Maracajaú; A. A. Aguiar for sharing unpublished data. Special thanks to all the long hours of laboratory work by student interns (F. Torquato and P. Pamplona). Finally, we acknowledge the financial support of Fundação Grupo Boticário de Proteção a Natureza.

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