The vulnerability of sharks is well known and cases of overexploitation have been documented around the world (Musick et al. 2000, Castro 2013). However, sustainable shark fisheries have been achieved in British Columbia and Australia as a result of rigorous management programmes (Walker 1998). The baseline of these programmes requires information about the biology of the species, as well as trends in fisheries. Unfortunately, in the Caribbean the local agencies have at their disposal poor information about elasmobranch fisheries, sometimes with similar species merged in a single item, so management decisions are limited (Shing 1999, Tavares 2009, Rosa and Gadig 2010).

In Venezuela, one of the most important resources in artisanal shark fisheries is the small-eye smooth-hound shark, Mustelus higmani Springer and Lowe, 1963, locally known as “viuda amarilla”. Between 1990 and 2006, shark landings in the northeastern region were 3000 t y^–1, with M. higmani accounting for around 40% of this catch (Tavares et al. 2010). This species is also an important resource in other Caribbean countries and Brazil (Lessa et al. 1999, Shing 1999, 2006). In Venezuela, sharks and rays are highly appreciated because they are included in typical dishes (Cervigón and Alcalá, 1999). The increasing local demand and economic value cause high fishing pressure on this resource. Although M. higmani is categorized as “least concern” by the red list of the International Union for Conservation of Nature, this estimation is only based on data from Brazil. Information about fisheries and population features throughout the distributional range is necessary to evaluate the current conservation status of this species (Faria and Furtado 2006).

Studies of M. higmani are mainly restricted to general descriptions (Compagno 1984, Cervigón et al. 1992, Cervigón and Alcalá 1999, Compagno et al. 2005) and taxonomical revisions (Heemstra 1997, Rosa and Gadig 2010). However, Springer and Lowe (1963) and Tavares et al. (2010) provide useful biological information.

We studied the landings from the artisanal fishery of Margarita Island between January 2006 and December 2008 in order to generate baseline information regarding reproduction and feeding habits that may contribute to update the conservation status of M. higmani.

Fishery managers should consider the temporal decrease in size and the increase in proportion of juveniles as symptoms of overexploitation of the stocks concerned, which therefore need specific monitoring plans. Powers et al. (2013) found a decrease in elasmobranch length in the Gulf of Mexico since 1980, associated with fisheries. Although the relative decrease in size in the present study is still low and the sampling period (three years) is not enough to detect robust trends, its combination with increases in the proportion of juveniles (up to 50% of the catches in 2008), could suggest a tendency towards the occurrence of suboptimal conditions for the fishery with the passing of time. Similar results with larger proportions of immature organisms in the catches were also observed by Tavares et al. (2010) in the same region and are also observed in other elasmobranchs caught by artisanal fisheries of Venezuela (Tavares 2009, Tagliafico et al. 2012, 2013).

Females of Mustelus higmani attain greater size than males (Compagno 1984, Cervigón and Alcalá 1999, Compagno et al. 2005), a common aspect for different species of the genus Mustelus, such as M. canis, M. norrisi (Cervigón and Alcalá 1999), M. antarcticus, M. griseus, M. lenticulatus, M. lunulatus, M. manazo, M. mustelus (Compagno et al. 2005) and M. punctulatus (Saidi et al. 2009). The largest body sizes previously reported for M. higmani were 75 cm and 59 cm TL for females and males, respectively (Tavares et al. 2010). The present work therefore reports a new maximum length, of 88.4 cm TL for females and 69.2 cm TL for males.

Temporal differences in population sex ratio suggest a low-scale spatial-temporal segregation. Springer and Lowe (1963) found an equal sex ratio in embryos, but reported the occurrence of some catches with just one sex. In the present study, occasional captures of a single sex (males o females) or combinations of adult females with young males were observed. Unfortunately, the lack of a defined pattern and the occurrence of mixed groups preclude testing the sexual segregation hypothesis. Saidi et al. (2008) reported similar results for M. mustelus, with a similar sex ratio for embryos and variation for adults.

Springer and Lowe (1963) report a length at maturity of about 47.5 and 42.5 cm TL for females and males, respectively. Tavares et al. (2010) reports a mean length at maturity of 59.9 cm TL for females and 52.5 cm TL for males. In contrast, we found a lower mean length at maturity (F=46.7 cm TL; M=47.6 cm TL). These differences can be attributed to different sample sizes and sampling periods. In general, for other species of the genus Mustelus, males mature before females, although some exceptions have been reported (Rojas 2006).

Occurrence of gravid and post-gravid females during the 26 months of the study, jointly with the occurrence of embryos in different stages of development, seems to show that M. higmani reproduce continually throughout the year. Springer and Lowe (1963) reported similar results by analysing 123 females, of which 106 were pregnant without any temporal pattern, with different embryo sizes. Similar records of pregnant females throughout the year were made for M. manazo in Japan (Yamaguchi et al. 2000), suggesting a non-fixed reproductive period similar to that of many tropical species, possibly due to the narrow seasonal variation of the environment.

The large ovum diameter observed for gravid and post-gravid females suggests that they could be ready to copulate and become gravid again after giving birth. A similar pattern has been reported for M. manazo, since females can become pregnant four to six weeks after giving birth (Yamaguchi et al. 2000).

Gestation period for other species of this genus is 10 months (M. griseus, M. canis and M. manazo), 11 months (M. antarcticus, M. lenticulatus and M. mustelus) and around one year (for M. asterias) (Compagno et al. 2005). In the present work, the continuous reproduction observed, with embryos that can be born at any time throughout the year, prevents us from estimating an accurate gestation period.

Female sharks commonly give birth near to the coast in order to raise survival probabilities of their offspring (Knip et al. 2010). This behaviour could explain the incidence of gravid females in the catches, as this artisanal fishery operates mainly in-shore. Gallucci et al. (2006) indicated that in these fisheries the risk of collapse of shark stocks increases because a large reproductive fraction of the population is captured annually. According to the current data, the risk could be even higher because catches also include a large proportion of juveniles.

A maximum fecundity of up to 10 embryos was suggested. However, this condition must be considered as rare, since it was observed in only one female, and pregnant females with more than seven embryos accounted for less than the 10% of gravid females. An average number of four embryos per female is similar to previous observations (Springer and Lowe 1963).

The smallest specimen observed in the landings (20 cm TL) was smaller than the largest embryo (29 cm), showing that first size of capture is similar to length at birth, due to the small mesh size of the net used, which makes it possible to catch all the available sizes. Also, some “early birth” of neonates, caused by the stress suffered by pregnant females caught by the nets, could be occurring. Springer and Lowe (1963) reported similar findings, with a catch of a neonate (21.3 cm TL) smaller than the largest recorded embryo (24 cm TL). This observation of neonate catches is also reported in shark fisheries from Africa and the Mediterranean Sea (Kroese and Sauer 1998, Saidi et al. 2008).

A similar length at birth has been reported for this species (25 cm TL) (Tavares et al. 2010). For other species of the genus Mustelus, the size between 19 and 21 cm TL has been indicated (M. dorsalis, M. minicanis and M. henlei). However, lengths above 30 cm TL have been observed for other species (M. antarcticus, M. asterias, M. canis, M. fasciatus, M. lunulatus, M. manazo, M. mento, M. mustelus, M. punctulatus and M. sinusmexicanus) (Compagno et al. 2005).

The previous data on the diet of M. higmani (Springer and Lowe 1963) report a similar picture to that identified in the present work. M. higmani’s food spectrum is based mainly on decapod crustaceans and stomatopods. Similarly, M. lunulatus, M. henlei, M. dorsalis, M. punctulatus, M. manazo and M. schmitti have a diet based on crustaceans (Yamaguchi and Tanuichi 2000, Gómez et al. 2003, Navia et al. 2006, Rojas 2006, Jardas et al. 2007, Saidi et al. 2009, Belleggia et al. 2012).

The large number of identified food items and the variation observed between different specimens suggests that M. higmani is an opportunistic nekto-benthic predator. Wetherbee et al. (1990) have indicated that in some elasmobranch species the stomach content varies according to environmental aspects and the abundance of preys. The identified preys suggest that this species consumes both benthic (epifaunal and infaunal species) and nekto-benthic preys, all commonly found on sandy bottoms of the continental shelf. Knip et al. (2010) suggests that small sharks frequently visit coastal zones to obtain prey in order to facilitate fast growth and quickly reach maturity length.

Crustaceans dominated the diet, but a considerable number of small clupeids (anchovies and sardines) that were identified could explain the low values in total weight of fishes. Also, some large remains of fish (possibly of the family Ariidae) were observed, suggesting that occasional large preys are trapped by some type of group hunt behaviour or scavenger feeding. Saidi et al. (2009) suggested the need for further research to corroborate the hypothesis of scavenger feeding for larger fish and to document ontogenic changes in the diet of M. punctulatus to consuming larger preys (like fish and molluscs) at greater sizes.

Trophic level decreases have been used to address overexploitation of resources in marine food webs (Pauly et al. 1998, Myers et al. 2007). Cortés (1999) estimated a trophic level for M. higmani of 3.6, which is slightly higher than the present estimation (3.3). This variation could be attributed to the presence of new rare items (algae, seagrass, octocorals, gastropods and polychaetes) possibly consumed by accident. Together, these food items represent less than 2% of the diet and could be considered trace food. For this reason, a new estimation of the trophic level was performed without including these items, resulting in the same trophic level reported by Cortés (1999). However, polychaetes, gastropods and vegetables have been previously reported as a common diet of this genus (Gómez et al. 2003, Jardas et al. 2007, Yamaguchi and Tanuichi 2000, Saidi et al. 2009, Belleggia et al. 2012), as well as echinoderms, bivalves and tunicates (Saidi et al. 2009).

There are noteworthy aspects of some observed food items. All hermit crabs (Paguridae and Diogenidae) were found without shells. Additionally, other consumed species inhabit galleries within sandy bottoms (thalassinideans and stomatopods) or hide themselves in sand (e.g. Calappidae and Parthenopidae crabs). Also, a large proportion of the preys were found complete (even intact) in the stomachs, and very few bite marks were observed. Based on these observations, we suggest that the species uses a suction mechanism to consume preys in sandy environments.

Other important findings about the diet of M. higmani are that it also includes the Indo-Pacific invasive species Charybdis hellerii. This portunid crab was observed in Venezuela in 1993 (Bolaños et al. 1997), and its distribution in the Atlantic includes Florida, the Caribbean Sea and Brazil (Campos and Türkey 1989, Lemaitre 1995, Mantelatto and Dias 1999). Along its distribution range in the Atlantic, C. hellerii is considered well established, forming dense populations on sandy habitats of both marine and estuarine coast (Bolaños et al. 2012, Sant’Anna et al. 2012). The occurrence of C. hellerii in the diet of M. higmani denotes that this species could play an important role as a natural predator of this invasive species.

Since M. higmani inhabits sandy environments of the continental platform, the current ban of the Venezuelan industrial trawl fishery (since 2009) could represent a sort of protection for its stocks. However, there is still a lack of other legal management measures to regulate the fishery of this important resource. Elevated proportions of immature specimens and gravid females in catches could represent a threat to the sustainable exploitation of the species. Most of the Venezuelan marine resources are currently recognized to be in a state of overfishing (Mendoza 2015), and several elasmobranch fisheries have already shown a lack of precautionary management. The occurrence of high percentages of immature individuals and pregnant females in elasmobranch catches (Tavares 2009, Tagliafico et al. 2012, 2013) must be avoided in order to preserve these valuable resources.

We therefore recommend the implementation of a continuous monitoring plan for the fishery targeting this species, aimed at obtaining useful information to properly manage this resource.