Mollusk bycatch in trawl fisheries targeting the Atlantic seabob shrimp Xiphopenaeus kroyeri on the coast of Sergipe, northeastern Brazil

The malacofauna bycatch of sea-bob shrimp Xiphopenaeus kroyeri (Heller, 1862) trawl fisheries on the coast of Sergipe was studied for 5 years. The malacofauna bycatch considered was obtained in nine oceanographic sampling campaigns carried out between May 1999 and June 2003 in 18 stations distributed in six transects along depths of 10, 20 and 30 m. A total of 2,669 individuals of mollusk belonging to 54 species were captured on the 18 sea-bob shrimp trawl stations carried out along the coast of Sergipe. The considerable richness of mollusks was composed by 19 families and 31 species of gastropods, 12 families and 19 species of bivalves and 2 families and 4 species of cephalopods. The highest abundance were observed at stations 13 (373 individuals) and 16 (685 individuals) that represents the lowest depth (10 m) and the richness was higher at stations 15 and 12 (17 and 11 species, respectively) both located at the highest depth (30 m). Cephalopods had high frequency of occurrence being collected in all the stations and by far the most abundant group with a total of 2,488 individuals captured. On the other hand, gastropods (with 142 individuals found in 83.3% of stations) and bivalves (about 1% of the individuals collected) contribute with a much smaller percentage of individuals captured. Lolliguncula brevis (Blainville, 1823) was most representative cephalopod in number and frequency of occurrence. Arcidae, Conidae, Muricidae and Strombidae were the families with the higher number of species in the trawl-fishery. Among bivalves, Pitar arestus (Dall & Simpson, 1901) and Spathochlamys benedicti (Verrill & Bush [in Verrill], 1897) were the species with higher frequency of occurrence. Although the considerable sample effort and a number of mollusks captured as bycath, the richness estimators indicated that the species richness could increase with additional sampling effort in the study area. The present study expands the taxonomic alpha knowledge on the mollusk bycatch of sea-bob shrimp trawl fisheries on the northeastern coast of Brazil. However, it is of crucial importance to assess urgently the negative impacts of the sea-bob shrimp trawl fisheries on the benthic community of the entire coast of Brazil. Key-Words. Megafauna; Mollusks; Gastropoda; Bivalvia; Cephalopoda.

Despite the environmental impact, these operations contribute to knowledge on metazoan richness in a given region through the study of the individuals captured. In Brazil, studies on the bycatch of coastal shrimp fisheries have been carried out mainly on fish fauna (Paiva-Filho & Schmiegelow, 1986;Braga et al., 2001;Graça-Lopes et al., 2002a;Branco & Verani, 2006a, b;Sedrez et al., 2013), whereas few studies have performed a refined qualitative and quantitative analysis of invertebrate groups in the bycatch (Graça- Lopes et al., 2002a;Branco & Fracasso, 2004;Branco & Verani, 2006b;Branco et al., 2015).
Shrimp trawling is practiced throughout the Brazilian Exclusive Economic Zone (Santos et al., 2006). In northeastern Brazil, about 1,560 motorized and non-motorized vessels operate along 3,413 km of coastline, exclusively exploiting populations of the family Penaeidae (Santos et al., 2006). The fishing and commercial exploitation of the Atlantic seabob Xiphopenaeus kroyeri (Heller, 1862) on the coast of Sergipe (northeastern Brazil) is one of the most important economic activities in the region (Guimarães & Landim, 2017). The participation of mollusk bycatch in such fisheries is usually high, surpassing many groups of invertebrates in terms of species richness. However, many of the mollusks caught are small and have no commercial value.
The present study represents the first effort to know the mollusk bycatch in shrimp trawl fisheries on the coast of the state of Sergipe and is an important step toward a better understanding of the diversity of the group on the continental shelf of the state. Besides that, this work aims to perform a qualitative and quantitative analysis of the mollusk bycatch in artisanal fishing operations targeting the Atlantic seabob on the coast of the state of Sergipe, northeastern Brazil.

Sampling design, identification and analysis
The fauna considered in this study was obtained during oceanographic sampling in nine campaigns carried out between May 1999and June 2003(May, August and December 1999March 2000;December 2001;June and December 2002;and June 2003). Eighteen stations between 10°36' to 11°21'S and 36°32' to 37°05'W were sampled (Table 1). These stations were distributed in six transects (a to f ) along depths of 10, 20 and 30 m (Fig. 1). Double trawls were performed using fishing trawlers with net sizes and mesh openings equal to those used by the local shrimp fishing fleet (mesh opening: 35 mm in the sleeves, 30 mm in the body and 25 mm in the drawer).
The material collected was processed immediately after sampling and deposited in the zoological collection of the Laboratório de Bentos Costeiro da Universidade Federal de Sergipe (CZUFS). Mollusks were separated from other taxa and identified mainly based on Rios (2009), Tunnell Jr. et al. (2010 and Redfern (2013). The trophic groups considered here are based on Rueda et al. (2009).
We estimated the richness and abundance at each station. The frequency of occurrence (FO%) of each taxa was determined by dividing the total number of stations that each taxa was found by the total number of stations with Mollusca and multiplying by 100. Taxa identified on the genus level were considered for the determination of richness when only one species of the genus was found.
We compared total observed richness to that expected using the Chao 1, first-order J jackknife (Jack 1) estimators and Bootstrap randomized 500 times on EstimateS (Version 9.1.0) (Colwell, 2013).
Images were obtained using a digital camera (Canon DSLR EOS Rebel T5i) and/or a stereoscopic microscope (Leica M205C and Leica Application Suit v4.4). Specimens were preserved in 70% ethanol and re-deposited at the scientific zoological collection of the Universidade Federal de Sergipe, Sergipe, Brazil (CZUFS).

RESULTS
The present study provides important insights regarding the composition of the mollusk fauna on the continental shelf off the state of Sergipe, Brazil, for which few data have been published thus far. During the study period, a total of 2,669 individuals belonging to 54 mollusk species were captured at 18 Atlantic seabob trawl stations along the coast of the state. This total was represented by 19 families and 31 species of gastropods (accounting for approximately 57.4% of the composition - Fig. 2, Table 2), 12 families and 19 species of bivalves (approximately 35.2% of the composition - Fig. 3, Table 3) as well as two families and four species of cephalopods (approximately 7.4% of the composition - Fig. 4, Table 4). The following taxa were not identified on the species level due to the poor state of preservation of the shells and/ or the fact that they were juveniles: Aplysia sp., Siratus sp. and Strombus sp. (Gastropoda); Chama sp., Chlamys sp., Corbula sp., Ostrea sp. and Spondylus sp. (Bivalvia); Loligo sp. and Octopus sp. (Cephalopoda). Tables 2-4 show the Mollusca richness obtained in each of the stations and respective depth sampled in this study as bycatch of trawl fisheries targeting the Atlantic seabob shrimp X. kroyeri on the coast of Sergipe.
The families with the highest numbers of species in the trawl fisheries on the coast of Sergipe were Arcidae, Conidae and Muricidae (each with three species) and Strombidae (four species). These four groups accounted for 24% of the species sampled. Calyptraeidae, Columbellidae and Turbinidae are families of gastropods, most known species of which have a shell length measuring between 5 and 37 mm. Due to this fact, we found only one to two species from each group retained in the net.
By far, cephalopods were the most abundant group, with a total of 2,488 individuals captured (93.21% of the total sampled) and a high frequency of occurrence, sampled at all stations (Table 4). Lolliguncula brevis was the most representative in number, biomass and frequency   of occurrence and was, by far, the most abundant lolliginid (2,381 individuals collected at 89% of stations) (Fig. 4B). Loligo sp. was the second most abundant lolliginid. Doryteuthis pleii and L. brevis co-occurred at nine stations, whereas Loligo sp. and L. brevis were sampled together at 10 stations, and D. pleii and Lolligo sp. co-occurred at six stations (Table 4). Among Octopodidae, Octopus sp. was sampled at only 16.66% of stations, whereas C. macropus (Fig. 4A) was caught at only one station (Table 4).
Gastropoda was the second most abundant group, with a total of 142 individuals caught at 83.3% of the stations (Table 2). Xenophora conchyliophora (Born, 1780) (Fig. 2T) predominated in abundance (43 individuals), although this species has been collected at four stations. Distorsio clathrata (Lamarck, 1816) (Fig. 2O) was the second most abundant species (35 individuals) collected at 55.55% of the stations, which was followed in abundance by V. cassiforme (Fig. 2R) with 17 individuals collected at three stations (16.66% - Table 2). Bivalves composed approximately 1% of the individuals caught in the trawl fisheries (Fig. 3), with a total of 31 individuals sampled at 61.11% of the stations (Table 3). Pitar arestus (Fig. 3K) and S. benedicti (Fig. 3H) had the highest frequency of occurrence (16.7%) in this group, although only four and three individuals were caught (Table 3), respectively.
Based on Rueda et al. (2009), the species of Mollusca studied here belong to five trophic groups: herbivores (macroalgae -N = 10), filter feeders (N = 21), carnivores (N = 24), carrion feeders and scavengers (N = 2). The xenophorid, aplysiid, turbinid, all strombids and the columbellid Columbella mercatoria represent some of the herbivorous gastropods identified. Only filter feeders were found among the bivalves, with gastropods of the family Calyptraeidae also included in this trophic group. All cephalopods and the majority of gastropods were carnivorous mollusks. Some of the gastropod carrion feeders and scavengers were ranellids and olivids.
Abundance was higher with the shallowest depth (10 m), whereas richness was greater at stations with the lowest depth (30 m). Stations 16 and 13 had the high-est abundance (685 and 373 individuals, respectively), whereas stations 15 and 12 had the greatest richness (17 and 11 species, respectively). Stations with a depth of 10 m were represented by 1,521 individuals and 12 species; stations with a depth of 20 m had a total of 739 individuals and 16 species and stations with a depth of 30 m had a total of 400 individuals and 38 species.

DISCUSSION
The lack of proper monitoring of the fishing fleet and the lack of data on the invertebrate bycatch of trawl fisheries along the coast of Brazil is extremely troublesome due to the impact of this highly predatory activity on communities of organisms, leading to a loss of Table 3. Bivalvia bycatch of trawl fisheries targeting the seabob shrimp Xiphopenaeus kroyeri on coast of Sergipe. The asterisk (*) means that the information about the station was lost for the taxa. biodiversity (Branco & Fracasso, 2004;Branco & Verani, 2006a). Despite the immense fishing pressure on shrimp stocks on the coast of Brazil, especially in the northeastern region of the country, few studies have addressed the benthic community captured as bycatch during such activities. For instance, only information about the crustaceans (Santos et al., 2016) has been published on the benthic invertebrate bycatch on the coast of the state of Sergipe, where shrimp trawling is an activity of considerable economic importance in the Exclusive Economic Zone (Guimarães & Landim, 2017). In our research, studies about the invertebrate bycatch in the Brazilian Exclusive Economic Zone are limited mainly to cnidarians, crustaceans, echinoderms and mollusks and generally are representative of southwest and south of Brazil (Pires-Vanin, 1992;Paiva et al., 2001;Graça-Lopes et al., 2002a, b;Branco & Fracasso, 2004;Branco & Verani, 2006a, b;De Léo & Pires-Vanin, 2006;Branco et al., 2015;Belz et al., 2018). Furthermore, some of those studies identified the invertebrates caught only on supra-specific level (Graça- Lopes et al., 2002b;Branco & Fracasso, 2004;Branco & Verani, 2006a, b). Mollusks constitute one of the most diverse groups of the benthic megafauna sampled during trawling activities (Pires-Vanin, 1992;De Léo & Pires-Vanin, 2006) and are among the main invertebrates accidentally caught in fisheries in Brazil (Pires-Vanin, 1992;Paiva et al., 2001;Branco & Verani, 2006a, b;Graça-Lopes et al., 2002a;Branco et al., 2015) as well as other coastal marine ecoregions around the world (Riestra et al., 2006;Prabhu et al., 2013;Öndes et al., 2018), in some cases, superseded in richness only by crustaceans (Graça-Lopes et al.,  Branco & Verani, 2006b;De Léo & Pires-Vanin, 2006). However, data on Mollusca bycatch are scarce in Brazil (Belz et al., 2018) and even non-existent in view of the numerous fishing activities developed on the Brazilian continental shelf, especially on the coast of the state of Sergipe, where studies about the group are limited to a few taxonomic and ecological approaches (Lima & Couto, 2001;Castro et al., 2005;Almeida et al., 2014;Lima et al., 2016).
In the present investigation, considerable richness of mollusk bycatch was found in trawl fisheries on the coast of Sergipe, especially when compared to previous studies. Belz et al. (2018) performed sampling for more than a year on the coast the state of Paraná (Pontal do Paraná) and recorded no more than 10 species in trawl fisheries targeting X. kroyeri. Branco et al. (2015) sampled 22 species of Mollusca on the coast of the state of Santa Catarina. Graça-Lopes et al. (2002a) identified 25 mollusks collected on the coast of the state of São Paulo. Costa & Di Beneditto (2009) found only eight species on the coast of the state of Rio de Janeiro.
The lolliginid, which was the most abundant taxon in the present study, seems to have similarities in terms of bathymetric and environmental requirements with the seabob shrimp X. kroyeri. Lolliguncula brevis occurs abundantly in shallow waters on the Brazilian coast and represented a large percentage of the bycatch of seabob shrimp fisheries in previous studies , Branco & Verani, 2006b).
The gastropods with higher abundance (D. clathrata, V. cassiforme and X. conchyliophora) were found mainly at depths of 20 and 30 m, which are on the continental shelf  off Sergipe. These locations are under less influence from the five estuarine regions and therefore receive a lower quantity of fine sediments. According to Diaz & Puyana (1994), Rios (2009) and Tunnell Jr. et al. (2010), D. clathrata can be collected on sandy substrates at depths between 20 and 300 m and V. cassiforme can be found at depths reaching 60 m (Rios, 2009). Xenophora conchyliophora is also reported on sandy substrates in shallow waters at depths between 2 and 85 m (Diaz & Puyana, 1994;Rios, 2009). However , Tunnell Jr. et al. (2010) reported this species at depths reaching 635 m depths on the coast of the state of Texas, USA. Gastropods are among the main components of benthic communities and occupy a number of ecological niches (Beesley et al., 1998;Tunnell Jr. et al., 2010). Although not abundant in the present study, the group undoubtedly has considerable ecological importance, especially in marine food chains, where they serve as filter feeders [e.g., calyptraeids], herbivores [e.g., C. mercatoria, L. costatus (Gmelin, 1791), Macrocypraea zebra (Linnaeus, 1758)], carnivores [e.g., C. reticulata, C. centurio, P. oculatus], carrion feeders and scavengers [e.g., A. circinata, C. variegata] (Tunnell Jr. et al., 2010). Gastropods also compete for food with other invertebrates, such as crustaceans and appear in the diet of other metazoans. The large number of carnivorous (including cephalopods), detritivores, carrion-feeding and scavenger marine gastropods found in this study strongly contrasts the small percentage of herbivorous species collected in the trawls. The functional groups recognized here based on trophic strategies are qualitatively similar those found by Branco et al. (2015) on the coast of the state Santa Catarina.
The richness of bivalves caught on the coast of Sergipe corresponds to about one third of the total composition of Mollusca. Considerable variation was found between the number of families and species of bivalves captured as bycatch in the present study and findings described for other Brazilian coastal zones. The richness of bivalves found here (12 families, 14 species and five other supra-specific taxa) is higher in comparison to the eight families and 10 species found by Graça- Lopes et al. (2002a) and five families and six species found by Branco et al. (2015) in Atlantic seabob trawl fisheries in the states of São Paulo and Santa Catarina, respectively. The Bivalvia species identified here and also found on the studies mentioned above were: Arcidae (Anadara notabilis (Röding, 1798)), Cardiidae (D. muricata) and Veneridae (P. arestus), respectively.
Each one of the species of bivalves corresponded to a small number of individuals and occurred at only one of the 18 stations, except Chama sp., S. benedicti and P. arestus, which were recorded at three (the first two species) and four (the last species) stations at depths of 20 to 30 m. The small number of bivalves sampled here and in the other studies mentioned could be due to the selectivity of the sampling method (trawls) as well as stations positioned at specific depths.
The mollusks caught on the coast of Sergipe do not have economic importance due the small size, small number of individuals captured or lack of commercial demand. Organisms caught during fishing activities that are not exploited economically, denominated 'trash, waste or discard' , are thrown back into the sea, mainly dead (Graça- Branco, 1999). This is one of the major economic and environmental problems in the maritime fishery sector and poses a threat to marine megafauna across the oceans of the world (Komoroske & Lewison, 2015).
The ecological implications of the frequency of occurrence found for the different groups of epibenthic and nektonic mollusks caught on the continental shelf off Sergipe remain little understood. Thus, the identification of mollusk bycatch in trawl fisheries is an important step toward evaluating the ecological importance of the organisms that are being captured and, consequently, the impact of this fishing activity along the coast of Brazil.
Among the mollusks studied, only C. centurio and C. jaspidea (Gmelin, 1791) are on the IUCN Red List of Threatened Species (2018), listed under the status "least concern". The other taxa identified here and analyzed in a few studies have not yet been assessed for the IUCN Red List. However, this does not mean that they are free of danger, as many species of mollusks (e.g., D. pleii, L. brevis and Z. dufresnei) are under intense indirect fishing pressure, accounting for tons of bycatch in trawl fisheries on the coast of Brazil (Pires-Vanin, 1992;Branco & Verani, 2006b;De Léo & Pires-Vanin, 2006;Graça-Lopes et al., 2002a, b;Branco et al., 2015).
Sampling efforts, seasonal dynamics, environmental characteristics and lifestyles exert a strong influence on the capture of mollusks on the coast of Sergipe. Moreover, the richness found in the present study was more than 50% of the richness estimated using the Chao 1, Jack 1 and Bootstrap methods, demonstrating that fishery trawls have low selectivity, making this a high impact sampling method.
The present study expands taxonomic alpha knowledge on the Mollusca bycatch of trawl fisheries targeting the Atlantic seabob X. kroyeri on the northeastern coast of Brazil. Despite this positive aspect, the biological and ecological disturbances caused by trawl fisheries and the direct effects on the community of mollusks and other benthic invertebrate groups need to be urgently studied on the Brazilian coast as well as other marine ecoregions worldwide.