The crustacean bycatch of seabob shrimp Xiphopenaeus kroyeri (Heller, 1862) fisheries in the Cananéia region, southern coast of São Paulo, Brazil

Regional Studies in Marine Science 31 (2019) 100799

Contents lists available at ScienceDirect

Regional Studies in Marine Science journal homepage: www.elsevier.com/locate/rsma

The crustacean bycatch of seabob shrimp Xiphopenaeus kroyeri (Heller, 1862) fisheries in the Cananéia region, southern coast of São Paulo, Brazil ∗

Gabriel Lucas Bochini a , , Gilson Stanski b , Antonio Leão Castilho b , Rogerio Caetano da Costa a a b

Department of Biological Sciences, Faculty of Sciences, UNESP – Univ Estadual Paulista, Bauru, SP, Brazil Department of Zoology, Institute of Biosciences, UNESP – Univ Estadual Paulista, Botucatu, SP, Brazil

article

info

Article history: Received 22 October 2018 Received in revised form 24 July 2019 Accepted 10 August 2019 Available online 13 August 2019 Keywords: Habitat sharing Decapoda Impact of trawling fisheries Crustacean

a b s t r a c t The bycatch of shrimp fisheries is highly diverse, but still understudied in the coast of Cananéia (São Paulo, Brazil), where shrimp fisheries are very intensive. Aiming to fill this gap, we analysed the diversity of crustaceans in the bycatch of seabob shrimp (Xiphopenaeus kroyeri) fisheries. Samplings were taken monthly, from March 2013 to May 2014, using a shrimp bottom trawling net aboard a commercial vessel. The crustacean bycatch encompassed 22 families, 36 genera and 46 species. The families with the highest species richness were Portunidae (8 species) and Penaeidae (5 species), corresponding to 17.4% and 10.9%, respectively, of all species caught. Overall, the abundance of X. kroyeri was higher than that of the crustacean bycatch except during in December 2013-February 2014, when the ratio was nearly 1:1 (Binomial test, p <0.05). There was a great variation in the abundance of crustaceans throughout the year, and the highest proportion of bycatch occurred outside the period when the fishery is forbidden. We provide evidence that the trawling in Cananéia captures a great diversity of crustaceans that coexist with the target shrimp species. © 2019 Elsevier B.V. All rights reserved.

1. Introduction Fisheries can lead to changes in biodiversity, especially in coastal areas (Ellingsen, 2001; Castilho et al., 2008), since they systematically remove the target organisms for commercial and subsistence purposes (Yodzis, 2001). The most obvious consequence of overfishing is the subsequent fish stock decline (Lewison et al., 2004). In addition, although much of the fishing effort targets one, or a group of, species, there are always impacts on other species (Slavin, 1983). Shrimp fisheries, for instance, are not selective and capture many other animals along with the target species, the so-called ‘‘bycatch species’’ (Samanta et al., 2018). The low selectivity of trawling results in a highly diverse bycatch, and in a high biomass, compared to the target species. Studies estimate that the bycatch biomass can be up to 11 times higher than the target’s biomass, leading to the discarding of tons of biological material worldwide each year (Rothschild and Gulland, 1982; Conolly, 1986). The discarded fauna is composed

∗ Corresponding author. E-mail address: [email protected] (G.L. Bochini). https://doi.org/10.1016/j.rsma.2019.100799 2352-4855/© 2019 Elsevier B.V. All rights reserved.

mainly of crustaceans, mollusks, fishes, echinoderms, and cnidarians (Lewison et al., 2004). Sometimes the bycatch volume constitutes an operational problem, besides resulting in the useless mortality of organisms that are returned dead or weakened, and interfering with the ecological balance of fishing areas (Severino-Rodrigues et al., 2002). Fortunately, a portion of the bycatch is marketable and can complement the fishing activity economically. In China, for instance, about 1.8 million tonnes of bycatch are used to feed the Chinese aquaculture industry (Zhou and Yimin, 1996). Although fishermen from other countries still discard it, in countries like Belize, Colombia, Costa Rica and Nicaragua it seems that 20%–30% of the once discarded bycatch is now exploited, and in Venezuela it is at least 30% (Clucas, 1997). Shrimp fisheries are one of the most important activities of the fishing economy in the southeastern coast of Brazil. The fishing industry in Cananéia, in the state of São Paulo, targets mollusks, fishes, and crustaceans, and it is the main livelihood of local communities. The fish and shellfish fisheries are divided into two major fleets: the industrial, that operates offshore, and the artisanal fleet, that operates within the coastal waters and estuarine lagoons (Mendonça and Katsuragawa, 2001; Mendonça and Miranda, 2008). In Cananéia, the seabob shrimp Xiphopenaeus kroyeri (Heller 1862) is the targeted penaeid, mainly due to its great abundance

2

G.L. Bochini, G. Stanski, A.L. Castilho et al. / Regional Studies in Marine Science 31 (2019) 100799

in coastal areas, and adequate body size. It is also easy to capture (Perez et al., 2001; Costa et al., 2007; Instituto de Pesca, 2018). X. kroyeri and other target species are caught by trawling, which is a non-selective and predatory method that destabilises the benthic communities (Ruffino and Castello, 1992; Branco and Fracasso, 2004). Several studies have addressed the crustaceans among the bycatch of different fisheries worldwide. For example, Costa et al. (2008) analysed the crustacean bycatch of bottom trawling in southern Portugal (Algarve). Queirolo et al. (2011) studied the use of alternative cod ends to reduce the crustacean bycatch of trawl fisheries in Chile. Pillai et al. (2014) analysed crustacean bycatch of trawl fisheries along the northern Tamil Nadu coast of India. Reed et al. (2017) studied the bycatch in Africa, and Varisco et al. (2017) in Argentina. In northeastern Brazil, Rodrigues-Filho et al. (2016) evaluated the seasonal cycles of the crustacean bycatch of seabob shrimp fisheries in northeastern Brazil, while Costa and Di Beneditto (2009), Di Beneditto et al. (2010) and Costa et al. (2016) studied the crustacean bycatch of seabob shrimp fisheries in the northern coast of Rio de Janeiro. Graça-Lopes et al. (2002a) and Mantelatto et al. (2016) analysed the composition and distribution of decapod crustaceans in the bycatch of X. kroyeri fisheries in the northern region of the state of São Paulo, while Graça-Lopes et al. (2002b) and Severino-Rodrigues et al. (2002) compared the composition of crustaceans in Perequê Beach, São Paulo. Along the coast of Santa Catarina, Branco and Fracasso (2004) analysed the occurrence and abundance of the crustacean bycatch, and Branco and Verani (2006) qualitatively and quantitatively analysed the ichthyofauna. All these studies reported a high species richness among the bycatch. Knowing the species composition of the bycatch of trawling fisheries in regions under intense fishing activity is essential for the development of successful management plans. Such knowledge is critical for the development of future mitigation strategies, and is needed to monitor the current ones, such as the fishing ban in the offseason period. In the south and southeast of Brazil, all fishing activities are prohibited during the offseason period that extends from March 01 to May 31 (Normative Ordinance No. 189/2008) (Ibama, 2008). Moreover, information on the species abundance and distribution is necessary to identify strategies that can improve the capture and management of the target species (Gabriel, 1992; Jay, 1996; Tyler et al., 1982). Therefore, the aim of the present study was to analyse the crustacean bycatch of seabob shrimp fisheries in Cananéia. 2. Materials and methods The lagoon-estuarine complex of Cananéia-Iguape is located at the southern end of the São Paulo coast (25◦ S–8◦ W), bounded on the north by the municipality of Iguape, on the east by Comprida Island, on the west by Serra do Mar and on the south by the islands of Cananéia and Cardoso. The complex presents two main connections with the ocean, through a single channel (Mar Pequeno-Barra de Icapara) to the north and, to the south, dividing into two branches (Cananéia Sea and Cubatão Sea-Trapandé Bay) which surround the Island of Cananéia. Tropical water, coastal water and central Atlantic water are the main water masses influencing the region (Matsuura, 1986). The samplings occurred monthly from March 2013 to May 2014 at four sampling sites of up to 15 m of depth (E1, E2, E3 and E4) (Fig. 1). The samplings ran until May 2014 to cover two offseason periods. For comparative purposes, the data were grouped into five 3-month periods: ‘‘Offseason 1’’ (March, April and May 2013), ‘‘Offseason 2’’ (March, April and May 2014), ‘‘Period 1’’ (June, July and August 2013), ‘‘Period 2’’ (September, October and November 2013), and ‘‘Period 3’’ (December 2013, January and February 2014). Samplings could not be conducted in

Mar/13 and Feb/14 due to unfavourable environmental conditions (strong winds and storms). The mean catch was calculated for each period and values were compared. A shrimp-fishing boat equipped with double-rig nets (mesh size 20 mm and 18 mm in the cod end) with openings between doors of 4.0 metres and a constant trawl speed of 2.0 knots was used for trawling. Each trawl lasted 30 min, covering a total area of 16,000 m2 . In the laboratory, the individuals were identified to species level. Penaeidae shrimps were identified according to Costa et al. (2003), Caridea shrimps according to Chace (1972), and Brachyura and Anomura following Melo (1996, 1999a, respectively). We obtained the number of individuals and weight (g) of each species. The mean number of individuals, per period and per species, was calculated for the crustacean bycatch and for X. kroyeri. Then, the ratio of X. kroyeri to bycatch, per period, was calculated as the quotient between the number of X. kroyeri and number of crustaceans in the bycatch. Deviations of the 1: 1 ratio were tested using the binomial test (α = 0.05) (Wilson and Hardy, 2002). The relative abundance (RA) was calculated (%) as the number of individuals of each species divided by the total number of individuals (excluding the target species X. kroyeri). The relative abundance was classified according to Graça-Lopes et al. (1993): very numerous (Vn) when above 5% of the total number captured; numerous (N) when between 1 and 5%; and not numerous (Nn) when below 1%. Regarding frequency of occurrence (FO) of each species in the samples, three categories were considered, following Dajoz’s scale (1983): Constant (Co) when present in more than 50% of the samples; accessory (Ace) when in between 25 and 50%; and accidental (Aci) when present in less than 25%. An Analysis of Variance (ANOVA 2-way), followed by Tukey post hoc test, was used to test for differences between seasons and stations. The level of significance was p < 0.05 (Zar, 1999). 3. Results The crustacean bycatch included 22 families, 36 genera and 46 species, in addition to X. kroyeri. Individuals were grouped into five taxonomic groups: Brachyura, Anomura, Penaeoidea, Caridea and Stomatopoda (Fig. 2). Overall, X. kroyeri was the most abundant species (85.14%), followed by Brachyura (10.53%), and Penaeoidea (3.24%). The other groups combined accounted for 1.09% (Fig. 3). The crustacean bycatch was composed of 70.82% of Brachyura, 21.82% of Penaeoidea, 4.32% of Caridea, 2.92% of Anomura and only 0.11% of Stomatopoda. The most representative families were: Portunidae, with eight species and 3679 individuals; Penaeidae, with five species and 999 individuals (excluding X. kroyeri); and Epialtidae, with four species and 130 individuals. Altogether, Portunidae and other Penaeidae accounted for more than 73.49% of the total crustacean bycatch (Table 1). In terms of frequency of occurrence in the samples, 20 species (43.48%) were constant (Co), 8 (17.39%) were accessory (Ace) and 18 (39.13%) were accidental (Aci). Concerning the abundance, five species (10.87%) were very numerous (Vn), 7 (15.22%) were numerous (N) and 34 (73.91%) were not numerous (Nn). Despite the large number of constant species in the samples (present in more than 50% of the samples), only five species were Vn (Table 1). Brachyura was the most abundant group, accounting for 70.82% (4508 ind.) of the total captured. There were 23 species of Brachyura, that is, 50% of the total species richness (Fig. 2). The highest abundances occurred in Offseason 2 (1755 ind.) and in Period 3

G.L. Bochini, G. Stanski, A.L. Castilho et al. / Regional Studies in Marine Science 31 (2019) 100799

3

Fig. 1. Map of the Cananéia region, in the state of São Paulo, Brazil. The labels E1, E2, E3 and E4 indicate the location of the sampling stations. The samplings took place from March 2013 to May 2014.

Fig. 2. Species richness of each crustacean taxonomic group in the bycatch of seabob shrimp Xiphopenaeus kroyeri (Heller 1862) fisheries in Cananéia, SP. Values above bars represent the total number of individuals per taxonomic group.

Fig. 3. Composition, in terms of percentage of each group (%), of the bycatch of seabob shrimp Xiphopenaeus kroyeri (Heller 1862) fisheries in Cananéia, SP, captured from March 2013 to May 2014.

(1574 ind.), while the lowest abundance occurred in Offseason 1 (136 ind.) (Table 1). Despite the high richness of Brachyura, 11 species were Aci and Fn, with less than 10 individuals captured. These species included accidental species or species usually not caught by trawling, such as Armases angustipes (Dana 1852), commonly found in mangroves, Stenorhynchus seticornis (Herbst 1788) and Menippe nodifrons Stimpson, 1859, found mainly in rocky shores, and the invasive Charybdis hellerii (A. Milne-Edwards, 1867) and Pyromaia tuberculata (Lockington, 1877).

Only seven species were constant during the study, and among these, three were very numerous: Callinectes danae Smith, 1869, with 2627 individuals, C. Ornatus Ordway, 1863, with 984 individuals, and Hepatus pudibundus (Herbst, 1785), with 491 individuals (Table 1). Penaeoidea was the second most abundant group. It represented 21.82% of the bycatch, with 1389 ind. distributed in seven species (15.22% of the total species) and three families (Penaeidae, Solenoceridae and Sicyoniidae). The largest catches occurred in

4

G.L. Bochini, G. Stanski, A.L. Castilho et al. / Regional Studies in Marine Science 31 (2019) 100799

Table 1 Abundance, total abundance (n), relative abundance (AR%) and frequency of occurrence (FO) of the non-target crustaceans caught with the seabob shrimp (Xiphopenaeus kroyeri (Heller, 1862)) in Cananéia, São Paulo, from March 2013 to May 2014. Vn = very numerous; N = numerous; Nn = not numerous; Co = Constant, Ace = accessory; Aci = accidental.

Penaeoidea

Caridea

Brachyura

Stomatopoda

Species

Offseason 1

Per 1

Per 2

Per 3

Offseason 2

Total

AR%

FO

Abundance

Penaeidae Artemesia longinaris Rimapenaeus constrictus Farfantepenaeus brasiliensis Farfantepenaeus paulensis Litopenaeus schmitti

0 31 0 1 16

0 132 8 2 75

26 15 13 7 4

7 162 73 125 18

0 5 44 24 211

33 345 138 159 324

0.52 5.42 2.17 2.50 5.09

Ace Co Co Co Co

Pn Mn N N Mn

Solenoceridae Pleoticus muelleri

0

6

160

27

0

193

3.03

Co

N

Sicyoniidae Sicyonia dorsalis

5

82

45

62

3

197

3.10

Co

N

Palaemonidae Leander paulensis Nematopalaemon schmitti Periclimenes paivai

1 1 6

3 1 3

1 0 0

0 0 0

0 0 0

5 2 9

0.08 0.03 0.14

Ace Aci Aci

Pn Pn Pn

Hippolytidae Exhippolysmata oplophoroides

185

15

8

45

3

256

4.02

Co

N

Alpheidae Alpheus SP

0

2

0

0

0

2

0.03

Aci

Pn

Ogyrididae Ogyrides SP

0

1

0

0

0

1

0.01

Aci

Pn

Portunidae Callinectes danae Callinectes ornatos Callinectes exasperatus Callinectes bocourti Callinectes sapidus Achelous spinimanus Arenaeus cribrarius Charybdis helleri

93 28 0 0 0 0 1 0

219 175 1 0 1 0 3 0

171 138 0 1 15 1 0 0

677 416 0 0 25 2 2 0

1467 227 0 0 12 3 0 1

2627 984 1 1 53 6 6 1

41.27 15.46 0.02 0.02 0.83 0.09 0.09 0.02

Co Co Aci Aci Co Ace Ace Aci

Mn Mn Pn Pn Pn Pn Pn Pn

Aethridae Hepatus pudibundus

6

82

112

263

28

491

7.71

Co

Mn

Leucosiidae Persephona mediterrânea Persephona punctata Persephona lichtensteinii

0 1 0

1 8 4

9 32 2

14 111 1

1 4 0

25 156 7

0.39 2.45 0.11

Co Co Ace

Pn N Pn

Epialtidae Libinia ferreirae Libinia spinosa Apiomithrax SP Notolopas brasiliensis

6 0 0 1

23 2 0 1

23 1 0 1

59 0 2 0

10 0 1 0

121 3 3 3

1.90 0.05 0.05 0.05

Co Aci Aci Aci

N Pn Pn Pn

Menippidae Menippe nodifrons

0

0

1

0

0

1

0.02

Aci

Pn

Pinnotheridae Dissodactylus crinitichelis

0

4

1

2

0

7

0.11

Ace

Pn

Inachoididae Pyromaia tuberculata

0

0

3

0

1

4

0.06

Ace

Pn

Dromiidae Hypoconcha arcuata

0

0

1

0

0

1

0.02

Aci

Pn

Inachidae Stenorhynchus seticornis

0

0

1

0

0

1

0.02

Aci

Pn

Sesarmidae Armases angustipes

0

0

1

0

0

1

0.02

Aci

Pn

Hymenosomatidae Teramnonotus monodi

0

4

1

0

0

5

0.08

Aci

Pn

Squillidae Squilla SP

1

3

2

0

1

7

0.11

Co

Pn

(continued on next page)

Period 3 with 474 individuals, followed by Period 1 with 305 individuals. Most species of Penaeoidea, except Sicyonia dorsalis Kingsley, 1878 and Rimapenaeus constrictus (Stimpson, 1871), are considered of economic importance. However, only Litopenaeus schmitti (Burkenroad, 1936) was Fr and Vn. Farfantepenaeus paulensis (Farfante Pérez, 1967) and F. brasiliensis (Latreille, 1817) were Fr and N, with 159 and 138 individuals, respectively.

Artemesia longinaris Spence Bate, 1888 is also of economic importance, but only 33 individuals were captured, characterising the species as Ace and Fn. R. constrictus was Fr and Vn, with 345 individuals captured. Regarding the Anomura, 186 individuals of nine species and three families were caught. The family Diogenidae was the most abundant with 96 individuals (51.61% of all anomurans). The

G.L. Bochini, G. Stanski, A.L. Castilho et al. / Regional Studies in Marine Science 31 (2019) 100799

5

Table 1 (continued).

Anomura

Species

Offseason 1

Per 1

Per 2

Per 3

Offseason 2

Total

AR%

FO

Abundance

Diogenidae Dardanus insignis Loxopagurus loxochelis Petrochirus Diógenes

4 3 1

7 26 0

3 10 3

1 10 4

17 2 5

32 51 13

0.50 0.80 0.20

Co Co Co

Pn Pn Pn

Paguridae Pagurus exilis Pagurus leptonix Pagurus criniticornis

1 8 3

15 32 0

5 10 0

2 0 0

1 1 0

24 51 3

0.38 0.80 0.05

Co Co Aci

Pn Pn Pn

Porcellanidae Porcellana sayana Minyocerus angustus Pisidia brasiliensis

0 0 0

5 0 1

3 2 0

0 0 0

1 0 0

9 2 1

0.14 0.03 0.02

Ace Aci Aci

Pn Pn Pn

Total carcinofauna

403

947

832

2110

2073

6365

100.00

Total: Xiphopenaeus kroyeri Carcinofauna: X. kroyeri (n)

13406 1 : 34

3596 1 : 4

5236 1 : 6

2542 1 : 1

11683 1 : 6

36463 1 : 6

highest abundance of Anomura occurred outside the offseason: Periods 1 and 2 had the highest abundances with 86 and 36 individuals, respectively. Although five species were Co, they appeared in small numbers and were therefore classified as Pn. In relation to Caridea, six species belonging to four families were collected, totalling 275 individuals (93.09% of the total carideans). Only Exhippolysmata oplophoroides (Holthuis, 1948) was Fr and N (256 individuals), while the others were Fn. The highest abundance occurred in Offseason 1, when 70.19% of carideans were collected (193 individuals). Stomatopoda was the least abundant group. Only one species of the genus Squilla Fabricius, 1787 was captured and classified as Fn (seven individuals) and Fr, being more abundant in Period 1 (three individuals), followed by Period 2 (two individuals). Overall, the abundance of X. kroyeri was higher than the bycatch. In Offseason 1, for instance, its abundance was 34 times higher than the bycatch (Table 1). In Period 3, however, the ratio was nearly 1:1 (Binomial test, p < 0.05, Fig. 4). The abundance of period 3 was significantly different from Offseason 1 and Offseason 2 (Tukey, p = 0.008). However, there were no statistical differences between seasons or stations (2-way ANOVA; P > 0.05). 4. Discussion The faunal inventories already conducted in Cananéia, including this study, have shown it has a very rich and well-established crustacean community (Santos et al., 2000; Mendonça and Katsuragawa, 2001; Ávila-Da-Silva et al., 2003; Mendonça, 2015). Among the several zoological groups in the bycatch, crustaceans are one of the most important in terms of abundance and species richness. This result evidences the need for more biological studies on the constant/very numerous species, which are still scarce in Cananéia. Our results showed a worrying relationship between the capture of the target species (X. kroyeri) and the resulting crustacean bycatch, especially considering the high species richness found. Fishing is the main economic activity in Cananéia, which was the second most productive fishing region in the state São Paulo in 2012 (Mendonça, 2015). Similar results, evidencing a high species richness in the bycatch, are found worldwide. For instance, Pillai et al. (2014) recorded 64 crustacean species in India. Costa et al. (2008), recorded that the bycatch represented 80% (in kg) of the target species’ biomass, in southern Portugal (Algarve). Zacharia et al. (2006) obtained 54% of bycatch in trawls. In Canada, the bycatch shrimp Pandalus borealis Kroyer, 1838 has been almost eliminated by trawl fisheries (Clucas, 1997). Shrimps, the main marine resource, are captured through bottom trawls, a non-selective method that destabilises benthic communities (Ruffino and Castello, 1992; Branco and Fracasso, 2004).

Thus, the excessive and continuous fishing activity can decrease the abundance and ultimately lead species to local extinction. Most of the time, individuals are returned dead or debilitated to the environment, and many of them are in reproductive stages (Severino-Rodrigues et al., 2002; Stanski and Castilho, 2016). As X. kroyeri is a dominant species in the benthic communities of the Brazilian coast, in certain times of the year its abundance is not only higher than that of the crustacean fauna, but higher than all the bycatch (Graça-Lopes et al., 2002a; Sedrez et al., 2013). This pattern was observed during most of our study period, e.g., during Offseason 1, the abundance of X. kroyeri was 30 times greater than the abundance of the crustacean bycatch. On the other hand, in Period 3, the quantities were very similar, with a ratio close to 1:1. There are two explanations for these results. The ratio seen in Period 3 is related to the life cycle of X. kroyeri. Spawning occurs mainly in spring and early summer (Heckler et al., 2014; Castilho et al., 2015), and, since this species exhibits the type 3 life cycle (Dall et al., 1990; Heckler et al., 2013), reproductive females migrate to deeper regions. Thus, the migration can explain the low abundance of X. kroyeri during Period 3 in the study area, which was also when the highest crustacean abundance was observed. On the other hand, the high abundance during the offseason is related to recruitment and is a consequence of the migration and spawning explained above. In the southeast of Brazil, recruitment commonly occurs in autumn, peaks in April (Costa et al., 2011; Heckler et al., 2014), and causes a significant population increase. During this period, the fishing ban protects the shrimps and causes the high abundance observed in the offseason. Thus, the offseason period evidently contributes to the maintenance of the stocks of X. kroyeri, and it is important for its protection. In contrast, soon after the offseason period, the intense fishing effort decreases the shrimp abundance and, consequently, its capture rates. The high bycatch observed in Period 3 is a worrying result, since the entire local fauna is unprotected and subjected to intense fishing. In this period, the high abundance of crustaceans in the bycatch might be due to the higher bottom water temperature. In the Cananéia region, the highest mean temperatures occur in summer, as it is a subtropical region with welldefined seasons (Garcia et al., 2018). High summer temperatures favour the reproduction of most crustacean species (Sastry, 1983; Rasheed and Mustaquim, 2010), and during this period, reproductive females of C. danae (the most abundant species in the bycatch) emigrate from the estuary to the bay for spawning Pita et al., 1985a,b; Negreiros-Fransozo and Fransozo, 1995; Chacur et al., 2000; Branco and Masunari, 2000; Chacur and NegreirosFransozo, 2001; Pereira et al., 2009; Araújo et al., 2011). In addition, other species that were very abundant in this period, such as C. ornatos, H. pudibundus, Persephona punctata and R. constrictus,

6

G.L. Bochini, G. Stanski, A.L. Castilho et al. / Regional Studies in Marine Science 31 (2019) 100799

Fig. 4. Proportion between the crustacean bycatch and Xiphopenaeus kroyeri, from March 2013 to May 2014, in the Cananéia-SP region. Black circles indicate deviations from the 1:1 ratio (Binomial Test, p < 0.05).

also use the shallow bay areas for reproduction (Miazaki et al., 2018). In spring and summer months, the South Atlantic Central Waters (SACW) can influence the coast of São Paulo and decrease bottom temperature to values below 20 ◦ C. The lower temperatures promote the migration of species more common in temperate and cold subtropical regions, such as Artemesia longinaris and Pleoticus muelleri (Costa et al., 2005; Castilho et al., 2008). Both species were present in Period 2, albeit at low abundances. In addition, in spring and summer, the primary productivity usually increases (Garcia et al., 2018), which coincides with the rainier seasons (Miyao et al., 1986). A higher precipitation increases the discharge of fresh water from the estuaries into the bay and creates favourable conditions for the establishment of organisms, such as more food resources and greater protection, due to increased water turbidity caused by increased sedimentation, and removal of predators (Alber, 2002). The increase in primary productivity influences the entire trophic web, thus increasing the biomass and abundance of the benthic community (Gonzalez-Rodriguez et al., 1992; Valentin and MonteiroRibas, 1993). Similar results have been found in the coast of São Paulo (Severino-Rodrigues et al., 2002), where the highest rates of crustacean bycatch occurred in spring and summer. In the coast of Santa Catarina, in Penha (Branco and Fracasso, 2004) and in São Francisco do Sul, the same was observed for Anomura (Stanski et al., 2016). Brachyura was the richest group, both in terms of species and family numbers . These results corroborated the studies by Zairion et al. (2018) in Indonesia, Queirolo et al. (2011) in Chile, and Pillai et al. (2014) in India. Along the Brazilian coast, examples include studies done in the complex bay–estuary of Santos and São Vicente-SP (Pita et al., 1985a), in Ubatuba-SP (Costa et al., 2016; Mantelatto et al., 2016), in Guarujá-SP (Severino-Rodrigues et al., 2002), in Penha-SC (Branco and Fracasso, 2004) and in Cananéia-SP (Severino-Rodrigues et al., 2009). In these localities, C. danae and C. ornatus were the most abundant and constant species in the fishing areas of X. kroyeri. They prefer habitats with low-to-moderate salinity, temperature slightly above 20 ◦ C, and muddy bottoms (Mantelatto and Fransozo, 1999; Reigada and Negreiros-Fransozo, 2001; Guerra-Castro et al., 2007). Such conditions are also preferred by X. kroyeri (Costa et al., 2007),

and were recorded by Garcia et al. (2018) in the Cananéia region during the same period, mainly in autumn and summer, when temperatures were above 23 ◦ C. These conditions, especially in relation to the granulometric composition of the sediment, also favour H. pudibundus, which was the third most abundant species in Cananéia. Near the coast, the sediment is thicker (Garcia et al., 2018), which explains the extensive abundance of H. pudibundus in this study. In addition, the increase in plant debris from the continent and brought in by the fresh water, contributes to the increase in the species abundance (Lima et al., 2014). In Cananéia, its highest abundance occurred in summer, a period of higher precipitation. Among Penaeoidea, R. constrictus was the most abundant shrimp species, followed by L. schmitti, F. paulensis and F. brasiliensis. The Cananéia region represents a natural nursery for these species, which exhibit the type 2 life cycle (Dall et al., 1990). The lagoon-estuarine complex, due to the conservation of its environmental conditions, is one of the main post-larvae breeding sites of penaeid shrimps (Chagas-Soares et al., 1995; Barioto et al., 2017). This is another important factor for the conservation of this region. The other taxonomic groups, Anomura, Caridea and Stomatopoda, comprised 16 species. Although their abundance is relatively low, their diversity in Cananéia is remarkable, especially when compared to the results obtained for these groups by Severino-Rodrigues et al. (2002) in Guarujá-SP, by Branco and Fracasso (2004) in Penha-SC, by Reigada et al. (2006) in the bay– estuary complex of Santos and São Vicente and by Junior et al. (2010) in Saco dos Limões, SC. 5. Conclusions This study shows that the bycatch of shrimp fisheries has a considerable fauna diversity. Bycatch discards represent a serious problem for the marine biodiversity, since not only the stocks of the bycatch species are affected, but the entire trophic networks (Harrington et al., 2005). The impacts caused by fauna mortality on the ecological balance of the fishing areas are still unknown (Severino-Rodrigues et al., 1985), but such mortality represents a valuable loss of food and biodiversity (Severino-Rodrigues et al., 1985; Branco and Verani, 2006). The sustainability of global fishery operations is of concern, not only due to the capture of the

G.L. Bochini, G. Stanski, A.L. Castilho et al. / Regional Studies in Marine Science 31 (2019) 100799

target species or those protected by public opinion, but also due to the discard of several species that could even be used as food resources in the future (Clucas, 1997). Further studies on the biology of the species found in this region are recommended, especially on those classified as very numerous and numerous, and because a high proportion of bycatch occurs outside the shrimp offseason period. Therefore, intense fishing pressure can unbalance species population sizes, which will directly affect the socioeconomic situation of the region. Acknowledgements This paper is part of the Thematic BIOTA-FAPESP (Sao Paulo Research Foundation) multidisciplinary research project, which is intended to produce a fine scale assessment of the marine decapod biodiversity in the state of Sao Paulo. Financial support for this project was provided by research grants from FAPESP 428, Brazil (Tematico Biota 429 2010/50188 − 8), CAPES, Brazil CIMAR II (# 23038.004310/2014 − 85), and scholarship funding, Brazil (process numbers 2015/20382 − 0 to LFM and 2014/01632 − 3 to SMS), and from the Brazilian National Council for Scientific and Technological Development (CNPq), Brazil (Regular Research 406006/2012 − 1 to RCC and Scholarship PQ-CNPq numbers of 305919/2014 − 8 and 306672/2018 − 9 to RCC and 308653/2014 − 9 awarded to ALC. References Alber, M., 2002. A conceptual model of estuarine fresh water inflow management. Estuar. Coast. Shelf Sci. 25 (6B), 1246–1261. http://dx.doi.org/10.1007/ BF02692222. Araújo, M.S.L.C., Negromonte, A.O., Barreto, A.V., 2011. Reproductive period of the swimming crab Callinectes danae at the Santa Cruz Channel, a highly productive tropical estuary in Brazil. Nauplius 19 (2), 155–162, http://www. scielo.br/pdf/nau/v19n2/a07v19n2.pdf. Ávila-Da-Silva, A.O., Carneiro, M.H., Mendonça, J.T., Servo, G.J.M., Bastos, G.C.C., Batista, P.A., 2003. Produção pesqueira marinha do litoral sul do estado de São Paulo no período de 1967 a 1994. In: Bol. Inst. Pesca, Série Relatórios Técnicos, São Paulo, vol. 13, pp. 1–24, http://www.pesca.sp.gov. br/propesq1994.pdf. Barioto, J.G., Stanski, G., Grabowski, R.C., Costa, R.C., Castilho, A.L., 2017. Ecological distribution of Penaeus schmitti (Dendrobranchiata: Penaeidae) juveniles and adults on the southern coast of São Paulo state, Brazil. Mar. Biol. Res. 13 (6), 693–703. http://dx.doi.org/10.1080/17451000.2017.1287923. Branco, J.O., Fracasso, H.A.A., 2004. Ocorrência e abundância da carcinofauna acompanhante na pesca do camarão sete-barbas Xiphopenaeus kroyeri Heller (Crustacea, Decapoda) na Armação do Itapocoroy, Penha, Santa Catarina, Brasil. Rev. Bras. Zool. 21 (2), 295–301. http://dx.doi.org/10.1590/S010181752004000200022. Branco, J.O., Masunari, S., 2000. Reproductive ecology of the blue crab, Callinectes danae Smith, 1869 in the Conceição Lagoon system, Santa Catarina Isle, Brazil. Rev. Bras. Zool. 60 (1), 17–27. http://dx.doi.org/10.1590/S003471082000000100004. Branco, J.O., Verani, J.R., 2006. Análise quali-quantitativa da ictiofauna acompanhante na pesca do camarão sete-barbas, na Armação do Itapocoroy, Penha, SC. Rev. Bras Zool. Curitiba, PR 23 (2), 381–391. http://dx.doi.org/10.1590/ S0101-81752006000200011. Castilho, A.L., Bauer, R.T., Freire, F.A.M., Fransozo, V., Costa, R.C., Grabowski, R.C., Fransozo, A., 2015. Lifespan and reproductive dynamics of the commercially important sea bob shrimp Xiphopenaeus kroyeri (Penaeoidea): synthesis of a 5-year study. J. Crust. Biol. 35 (1), 30–40. http://dx.doi.org/10.1163/ 1937240X-00002300. Castilho, A.L., Pie, M.R., Fransozo, A., Pinheiro, A.P., Costa, R.C., 2008. The relationship between environmental variation and species abundance in shrimp community (Crustacea: Decapoda: Penaeoidea) in south-eastern Brazil. J. Mar. Biol. Assoc. UK 88 (1), 119–123. http://dx.doi.org/10.1017/ S0025315408000313. Chace, Jr., F.A., 1972. The shrimps of the Smithsonian–Bredin Caribbean expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). In: Smithsonian Contributions to Zoology, vol. 98, pp. 1–179, http://C:/Users/Sony/Downloads/SCtZ-0098-Lo_res.pdf. Chacur, M.M., Mansur, C.B., Negreiros-Fransozo, M.L., 2000. Distributional patterns, seasonal abundance and moult cycle of Callinectes danae Smith, 1869 in the Ubatuba region, Brazil. Nauplius 8 (2), 215–226, http://www.crustacea. org.br/wp-content/uploads/2014/02/nauplius-v08n2a06Chacur.et_al_pdf.

7

Chacur, M.M., Negreiros-Fransozo, M.L., 2001. Distribuições espaciais e sazonais de Callinectes danae (Decapoda, Portunidae) na Baía de Ubatuba, São Paulo, Brasil. J. Crust. Biol. 21 (2), 414–425. http://dx.doi.org/10.1651/02780372(2001)021[0414:SASDOC]2.0.CO;2. Chagas-Soares, F., Pereira, O.M., Santos, E., 1995. Contribuição ao ciclo biológico de Penaeus schmitti, Burkenroad, 1936, Penaeus brasiliensis, Latreille, 1817 e Penaeus paulensis, Pérez-Farfante, 1967, na região lagunar-estuarina de Cananéia, São Paulo, Brasil. Bol. Inst. Pesca. 22 (1), 49–59, http://www.pesca. sp.gov.br/B_22_1_49-59.pdf. Clucas, I., 1997. A Study of the Options for Utilization of Bycatch and Discards from Marine Capture Fisheries. FAO, Rome, 59p. http://www.fao.org/docrep/ W6602E/w6602E00htm. Conolly, P.C., 1986. Status of the Brazilian shrimp fishing operations and results of related research. FAO General Contribution (3), 1– 28, http://www.icmbio.gov.br/cepsul/images/stories/biblioteca/download/ eventos_cientificos/conf_%201986_braz_shrimp_fishing.pdf. Costa, R.C., Carvalho-Batista, A., Herrera, D.R., Pantaleão, J.A.F., Teodoro, S.S.A., Davanso, T.M., 2016. Carcinofauna acompanhante da pesca do camarãosete-barbas Xiphopenaeus kroyeri em Macaé, Rio de Janeiro, sudeste brasileiro. Bol. Inst. Pesca 42 (3), 61–624. http://dx.doi.org/10.20950/16782305.2016v42n3p611. Costa, I.D., Di Beneditto, A.P.M., 2009. Caracterización preliminary de los invertebrados bentónicos capturados accidentalmente em la pesca de camarones en el Norte del estado de Río de Janeiro, Sudeste de Brasil. Lat. Am. J. Aquatic. Res. 37, 259–264. http://dx.doi.org/10.4067/S0718-560X2009000200013. Costa, M.E., Erzini, K., Borges, T.C., 2008. Bycatch of crustacean and fish bottom trawl fisheries from southern Portugal (Algarve). Sci. Mar. 72 (4), 801–814. http://dx.doi.org/10.3989/scimar.2008.72n4801. Costa, R.C., Fransozo, A., Freire, A.M., Castilho, A.L., 2007. Abundance and ecological distribution of the ‘‘sete-barbas’’ shrimp Xiphopenaeus kroyeri (Heller, 1862) (Decapoda: Penaeoidea) in three bays of the Ubatuba region, southeastern Brazil. Gulf and Caribbean Reser. 19 (19), 33–41. http://dx.doi. org/10.18785/gcr.1901.04. Costa, R.C., Fransozo, A., Melo, G.A.S., Freire, F.A.M., 2003. An illustrated key for Dendrobranchiata shrimps from the northern coast of São Paulo state, Brazil. Biota Neotropica 3 (1), 1–12. http://dx.doi.org/10.1590/S167606032003000100011. Costa, R.C., Fransozo, A., Negreiros-Fransozo, M.L., 2005. Ecology of the rock shrimp Sicyonia dorsalis Kingsley, 1878 (Crustacea: Sicyoniidae) in a tropical region of Brazil. Gulf and Caribben Res. Ocean. Springs 17 (1), 49–56. http://dx.doi.org/10.18785/gcr.1701.05. Costa, R.C., Heckler, G.S., Simões, S.M., Lopes, M., Castilho, A.L., 2011. Seasonal variation and environmental influences on abundance of juveniles of the seabob shrimp Xiphopenaeus kroyeri (Heller, 1862) in southeastern Brazil. In: Pessani, D., Tirelli, T., Froglia, C. (Eds.), IX Colloquium Crustacea Mediterranea – Behaviour, Ecology, Fishery. Monografie del Museo Regionale di Scienze Naturali, Torino, Italy, pp. 47–58. Dajoz, R., 1983. Ecologia Geral. Editora Vozes, EDUSP, São Paulo, 472 p. Dall, W., Hill, B.J., Rothilsberg, P.C., Staples, D.J., 1990. The biology of the penaeidae. In: Blaxteer, J.H.S., Southward, A.J. (Eds.), In: Advances in Marine Biology, vol. 27, Academic Press, San Diego, pp. 1–1489. Di Beneditto, A.P.M., De Souza, G.V.C., Tudesco, C.C., Klôh, A.S., 2010. Records of brachyuran crabs as bycatch from the coastal shrimp fishery in northern Rio de Janeiro State. Brazil. Mar. Biod. Rec. 3 (77), http://dx.doi.org/10.1017/ S1755267210000679. Ellingsen, K.E., 2001. Biodiversity of a continental shelf soft-sediment macrobenthos community. Mar. Ecol. Prog. Ser. 218, 1–15. http://dx.doi.org/10.3354/ meps218001. Gabriel, W.L., 1992. Persistence of demersal fish assemblages between Cape Hatteras and Nova Scotia, north-west Atlantic. J. Northwest Atl. Fish. 14, 29–46, http://journal.nafo.int/Portals/0/1992-3/gabriel.pdf. Garcia, J.R., Lopes, A.E.B., Silvestre, A.K.C, Grabowski, R.C., Barioto, J.G., Costa, R.C., Castilho, A.L., 2018. Environmental characterization of the Cananéia coastal area and its associated estuarine system (São Paulo state, Brazil): Considerations for three Penaeoidean shrimp species. Reg. Stud. Mar. Sci. 19, 9–16. http://dx.doi.org/10.1016/j.rsma.2018.02.010. Gonzalez-Rodriguez, E., Valentin, J.L., Andre, D.L., Jacob, S.A., 1992. Upwelling and pownwelling at Cabo Frio (Brazil): comparision of biomass and primary production responses. J. Plankton Res. 14 (2), 289–306. http://dx.doi.org/10. 1093/plankt/14.2.289. Graça-Lopes, R., Puzzi, A., Severino-Rodrigues, E., Bartolotto, A.S., Guerra, D.S.F., Figueiredo, K.T.B., 2002b. Comparação entre a produção de camarão-setebarbas e de fauna acompanhante pela frota-de-pequeno-porte sediada na Praia de Perequê, Estado de São Paulo, Brasil. Bol. Inst. Pesca, São Paulo, Brasil. 28 (2), 189–194, http://www.pesca.sp.gov.br/28_2_189-194.pdf. Graça-Lopes, R., Severino-Rodrigues, E., Puzzi, A., Pita, J.B., Coelho, J.A.P., Freitas, M.L., 1993. Levantamento ictiofaunístico em um ponto fixo na baía de Santos, Estado de São Paulo, Brasil. Bol. Inst. Pesca, São Paulo. 20, 7–20, http://www.pesca.sp.gov.br/20_01_unico_7-20.pdf.

8

G.L. Bochini, G. Stanski, A.L. Castilho et al. / Regional Studies in Marine Science 31 (2019) 100799

Graça-Lopes, R., Tomás, A.R.G., Tutui, S.L.S., Severino-Rodrigues, E., Puzzi, A., 2002a. Fauna acompanhante da pesca camaroneira no litoral do Estado de São Paulo, Brasil. Bol. Inst. Pesca 28, 173–188, https://www.pesca.sp.gov.br/ 28_2_173-188.pdf. Guerra-Castro, E., Carmona-Suérez, C.A., Conde, J.E., 2007. Activity patterns and zonation of the swimming crabs Arenaeus cribarius and Callinectes ornatus. J. Crust. Biol. 27 (1), 49–58. http://dx.doi.org/10.1651/S-2651.1. Harrington, J.M., Myers, R.A., Rosenberg, A.A., 2005. Wasted fishery resources: discarded by-catch in the USA. Fish Fish 6 (4), 350–361. http://dx.doi.org/10. 1111/j.1467-2979.2005.00201.x. Heckler, G.S., Costa, R.C., Fransozo, A., Rosso, S., Shimizu, R.M., 2014. Long-term patterns of spatial and temporal distribution in the seabob shrimp Xiphopenaeus kroyeri (Decapoda: Penaeidae) population in Southeastern Brazil. J. Crust. Biol. 34 (3), 326–333. http://dx.doi.org/10.1163/1937240X-00002231. Heckler, G.S., Simões, S.M., Lopes, M., Zara, F.J., Costa, R.C., 2013. Biologia Populacional e Reprodutiva do camarão sete-barbas na baía de Santos, São Paulo. Bol. Inst. Pesca São Paulo. 39 (3), 283–297, http://www.pesca.sp.gov. br/39_3_283-297.pdf. Ibama, 2008. Normative Instruction No. 189 of September 23, 2008. In: Process IBAMA/SC No 2026.001828/. Final meeting with representations of the Southeast and South regions, held in Itajaí / SC, on August 21, 2008. pp. 2005–2035, http://www.icmbio.gov.br/cepsul/images/stories/legislacao/ Portaria/2008/in_ibama_189_2008_regulamenta_pesca_camaroes_defeso_se_ s.pdf. (Acesso 18/09/2018). Instituto de Pesca, 2018. Produção Pesqueira Marinha e Estuarina do Estado de São Paulo. Instituto de Pesca Informe Pesqueiro de São Paulo, São Paulo. 91. pp. 1–4, http://www.propesq.pesca.sp.gov.br/arquivos/pagina/1550282120_ InfoPesqSP091_InformePMAP1711.pdf. Jay, C.V., 1996. Distribution of bottom-trawl fish assemblages over the continental shelf and upper slope of the U.S. west coast, 1977–1992. Can. J. Fish. Aquat. Sci. 53, 1203–1225. http://dx.doi.org/10.1139/f96-055. Junior, F.F., Christoffersen, M.L., Branco, J.O., 2010. Monitoring of carcinofauna abundance and diversity during eight years of expressway construction in Santa Catarina, Brazil. Lat. Am. J. Aquat. Res. 38 (3), 461–473. http://dx.doi. org/10.3856/vol38-issue3-fulltext-10. Lewison, R.L., Crowder, L.B., Read, A.J., Freeman, S.A., 2004. Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol. Evolut. 19 (11), 598–604. http://dx.doi.org/10.1016/j.tree.2004.09.004. Lima, P.A., Fransozo, V., Andrade, L.S., Almeida, A.C., Furlan, M., Fransozo, A., 2014. Distribution and population structure of the flecked box crab Hepatus pudibundus (Decapoda, Brachyura) in the western South Atlantic. Mar. Biol. Res. 10 (6), 589–600. http://dx.doi.org/10.1080/17451000.2013.841940. Mantelatto, F.L.M., Bernardo, C.H., Silva, T.E., Bernardes, V.P., Cobo, V.J., Fransozo, A., 2016. Composição e distribuição de crustáceos decápodes associados à pesca do camarão-sete-barbas Xiphopenaeus kroyeri (Heller, 1862) no litoral norte do estado de São Paulo. Bol. Inst. Pesca. 42 (2), 307–326. http://dx.doi.org/10.20950/1678-2305.2016v42n2p307. Mantelatto, F.L.M., Fransozo, A., 1999. Reproductive biology and moulting cicle of the crab Callinectes ornatus (Decapoda, Portunidae) from the Ubatuba region, São Paulo, Brazil. Crustaceana, Leiden 72 (1), 63–76. Matsuura, Y., 1986. Contribuição ao estudo da estrutura oceanográfica da região sudeste entre Cabo Frio (RJ) e Cabo de Santa Marta Grande (SC). Ciência e Cultura 38 (8), 1439–1450. Melo, G.A.S., 1996. Manual de identificação dos Brachyura (Caranguejos, Siris) do litoral Brasileiro. 604p. Plêiade / FAPESP, São Paulo, SP, Brasil. Melo, G.A.S., 1999a. Manual de identificação dos crustacea Decapoda do litoral brasileiro: Anomura, Thalassinidea, Palinuridea E Astacidea. Editora Plêiade, São Paulo. Mendonça, J.T., 2015. Caracterização da pesca artesanal no litoral sul de São Paulo –Brasil. Bol. Inst. Pesca 41 (3), 479–492. Mendonça, J.T., Katsuragawa, M., 2001. Caracterização da pesca artesanal no complexo estuarino-lagunar de Cananéia-Iguape, Estado de São Paulo, Brasil (1995-1996). Acta Sci. 23 (2), 535–547. http://dx.doi.org/10.4025/ actascibiolsci.v23i0.2713. Mendonça, J.T., Miranda, L.V., 2008. Estatística pesqueira do litoral sul do estado de São Paulo: subsídios para gestão compartilhada. Pan-Am. J. Aquat. Sci 3, 152–173, http://www.panamjas.org/pdf_conteudos/PANAMJAS_3(3)_152173.pdf. Miazaki, L.F., Simões, S.M., Castilho, A.L., Costa, R.C., 2018. Population dynamics of the crab Hepatus pudibundus (Herbst, 1785) (Decapoda, Aethridae) on the southern coast of São Paulo state, Brazil. J. Mar. Biol. Assoc. UK http: //dx.doi.org/10.1017/S0025315418000620. Miyao, S.Y., Nishihara, L., Sarti, C.C., 1986. Características físicas e químicas do sistema estuarino-lagunar de Cananéia-Iguape. Bol. Inst. Ocean. São Paulo 34, 23–36. http://dx.doi.org/10.1590/S0373-55241986000100003. Negreiros-Fransozo, M.L., Fransozo, A., 1995. On the distribution of Callinectes ornatus Ordway, 1863 and Callinectes danae Smith, 1869 (Brachyura, Portunidae) in the Fortaleza Bay, ubatuba, brazil. Iheringia, Série Zool. 79, 13–25.

Pereira, M.J., Branco, J.O., Christoffersen, M.L., Freitas Júnior, F., Fracasso, H.A.A., Pinheiro, T.C., 2009. Population biology of Callinectes danae and Callinectes sapidus (Crustacea: Brachyura: Portunidae) in the south-western Atlantic. J. Mar. Biol. Assoc. UK 89, 1341–1351. http://dx.doi.org/10.1017/ S0025315409000605. Perez, J.A.A., Pezzuto, P.R., Rodrigues, L.F., Valentini, H., Vooren, C.M., 2001. Relatório da Reunião Técnica de Ordenamento da Pesca de Arrasto nas regiões Sudeste e Sul do Brasil. In: NotasTécnicas da FACIMAR, vol. 5, pp. 3–34, https://siaiap32.univali.br/seer/index.php/bjast/article/viewFile/2505/1726. Pillai, S.L., Kizhakudan, S.J., Radhakrishnan, E.V., Thirumilu, 2014. Crustacean bycatch from trawl fishery along north Tamil Nadu coast. Indian J. Fish. 61 (2), 7–13, http://epubs.icar.org.in/ejournal/index.php/IJF/article/view/29663/ 19108. Pita, J.B., Severino Rodrigues, E., Graça-Lopes, R., Coelho, J.A.P., 1985a. Levantamento da família Portunidae (Crustacea, Decapoda, Brachyura) no Complexo Baía-Estuário de Santos, S. Paulo, Brasil. Bol. Inst. Pesca 12 (3), 153–162, http://www.pesca.sp.gov.br/sumario_12_3_153-162.pdf. Pita, J.B., Severino-Rodrigues, E., Graça-Lopes, R., Coelho, J.A.P., 1985b. Observações bioecológicas sobre o siri Callinectes danae no Complexo Baía/Estuário Santos, São Paulo. Brasil. Bol. Inst. Pesca 12 (4), 35–43. Queirolo, D., Erzini, K., Hurtado, C.F., Ahumada, M., Soriguer, M.C., 2011. Alternative codends to reduce bycatch in Chilean crustacean trawl fisheries. Fish. Res. 110, 18–28. http://dx.doi.org/10.1016/j.fishres.2011.03.005. Rasheed, S., Mustaquim, J., 2010. Size at sexual maturity, breeding season and fecundity of three-spot swimming crab Portunus sanguinolentus (Herbst, 1783) (Decapoda, Brachyura, Portunidae) occurring in the coastal waters of Karachi, Pakistan. Fish. Res. 103, 56–62. http://dx.doi.org/10.1016/j.fishres. 2010.02.002. Reed, J.R., S.E.K.erwath, S.E., Attwood, C.G., 2017. Analysis of bycatch in the South African midwater trawl fishery for horse mackerel Trachurus capensis based on observer data. Afr. J. Mar. Sci. 39 (3), 279–291. Reigada, A.L., Negreiros-Fransozo, M.L., 2001. Feeding activity of Callinectes ornatus Ordway, 1863 and Callinectes danae Smith, 1869 (Crustacea, Brachyura, Portunidae) in Ubatuba, SP, Brazil. Hydrobiologia 449, 249–252. http://dx. doi.org/10.1023/A:1017563119813. Reigada, A.L.D., Toyama, M.H., Serrano, J.S., Alves, R.M.S., Zara, F.J., 2006. Macrocrustaceans of non-consolidated sublittoral of the São Vicente Estuarine Bay Complex, São Paulo state, Brazil. Check List 2, 84–88. http://dx.doi.org/10. 15560/2.3.84. Rodrigues-Filho, J.L., Couto, E.C.G., Barbieri, E., Branco, J.O., 2016. Ciclos sazonais da carcinofauna capturada na pesca do camarão–sete-barbas, Xiphopenaeus kroyeri no litoral de Santa Catarina. Bol. Inst. Pesca. 42 (3), 648–661. http: //dx.doi.org/10.20950/1678-2305.2016v42n3p648. Rothschild, B.J., Gulland, J.A., 1982. Interim Report of the Workshop on the Scientific Basis for the Management of Penaeid Shrimp. NOAA, Technical. Memorandum, NMFS-SEFC. Ruffino, M.L., Castello, J.P., 1992. Alterações na Ictiofauna acompanhante da pesca do camarão-barba-ruça (Artemesia longinaris) nas imediações da Barra de Rio Grande, Rio Grande do Sul – Brasil. Nerítica 7 (1–2), 43–55, https://www.researchgate.net/publication/265594676_Alteracoes_ na_ictiofauna_da_pesca_do_camarao-barbaruca_Artemesia_longinaris_nas_ imediacoes_da_Barra_do_Rio_Gr{and}e_Rio_Gr{and}e_do_Sul_Brasil. (Access 18/09/2018). Samanta, R., Chakraborty, S.K., Shenoy, L., Nagesh, T.S., Behera, S., Bhoumik, T.S., 2018. Bycatch characterization and relationship between trawl catch and lunar cycle in single day Shrimp Trawls from Mumbai Coast of India. Reg. Stud. Mar. Sci. 17, 47–58. http://dx.doi.org/10.1016/j.rsma.2017.11.009. Santos, S., Negreiros-Fransozo, M.L., Fransozo, A., 2000. The distribuition of the swimming crab Portunus spinimanus Latreille, 1819 (Crustacea, Brachyura, Portunidae) in Fortaleza bay, Ubatuba, SP, Brazil. Atlantica 16, 125–141, htt p://C:/Users/Sony/Downloads/1994.Santosetal.Thedistributionoftheswimming crabPortunusspinimanusLatreille1819CrustaceaBrachyur-PETI3MOS.pdf. Sastry, A.N., 1983. Ecological aspects of reproduction. Biol. Crust. 8, 179–270, https://zookeys.pensoft.net/articles.php?id=4263. Sedrez, M.C., Branco, J.O., Freitas Junior, F., Monteiro, H.S., Barbireri, E., 2013. Ictiofauna acompanhante na pesca artesanal do camarão sete-barbas (Xiphopenaeus kroyeri) no litoral sul do Brasil. Biota Neotrop 13 (1), 165–175. http://dx.doi.org/10.1590/S1676-06032013000100019. Severino-Rodrigues, E., Guerra, D.S.F., Graça-Lopes, R., 2002. Carcinofauna acompanhante da pesca dirigida ao camarão sete-barbas (Xiphopenaeus kroyeri) desembarcada na praia do Perequê, estado de São Paulo, Brasil. Bol. Inst. Pesca. 28 (1), 33–48, http://www.pesca.sp.gov.br/instituto%20de%20pesca% 2033-48.pdf. Severino-Rodrigues, E., Pita, J.B., Graça-Lopes, R., Coelho, J.A.P., 1985. Levantamento das espécies de camarões presentes no produto da pesca dirigida ao camarão-sete-barbas (Xiphopenaeus kroyeri) no Estado de São Paulo, Brasil. Bol. Inst. Pesca 12 (4), 77–85, http://www.pesca.sp.gov.br/sumario_12_4_7785.pdf.

G.L. Bochini, G. Stanski, A.L. Castilho et al. / Regional Studies in Marine Science 31 (2019) 100799 Severino-Rodrigues, E., Soares, F.C., Graça-Lopes, R., Souza, K.H., Canéo, V.O.C., 2009. Diversidade e biologia de espécies de Portunidae (Decapoda, Brachyura) no estuário de Iguape, Ilha Comprida e Cananéia, São Paulo, Brasil. Bol. Inst. Pesca. 35 (1), 47–60, http://www.pesca.sp.gov.br/35_1_47-60.pdf. Slavin, J.W., 1983. Utilización de la pesca acompanhante del camarón. In: IDRC. Pesca Acompañante – Un Regalo Del Mar: informe de uma consulta técnica sobre utilización de la pesca acompañante del camarón celebrada em Georgetown, Guyana. Ottawa. pp. 67–71, https://idl-bnc-idrc.dspacedirect. org/bitstream/h{and}le/10625/21173/IDL-21173.pdf?. Stanski, G., Castilho, A.L., 2016. Reproductive biology of the hermit crab Isocheles sawayai (Crustacea, Anomura) from coastal waters of Southern Brazil. Invertebr. Reprod. Dev. 60 (2), 103–111. http://dx.doi.org/10.1080/07924259.2016. 1160001. Stanski, G., Mantelatto, F.L., Castilho, L.C., 2016. Hermit crab bycatch fauna (Decapoda, Anomura) off the coast of Santa Catarina State, Brazil: diversity and spatial–temporal distribution. Lat. Am. J. Aquat. Res. 44 (3), 546–556. http://dx.doi.org/10.3856/vol44-issue3-fulltext-13. Tyler, A.V., Gabriel, W.L., Overholtz, W.J., 1982. Adaptive management based on structure of fish assemblages of northern continental shelves. In: Mercer, M.C. (Ed.), In: Multispecies Approaches to Fisheries Management Advice, vol. 59, Canad. Spec. publ. fish. Aquat. Sci., pp. 149–156, http://www.dfompo.gc.ca/Library/51291.pdf. Valentin, J.L., Monteiro-Ribas, W.M., 1993. Zooplankton community structure on the east-southeast Brazilian continental shelf (18–23◦ S latitude). Cont. Shelf. Res. 13 (4), 407–424. http://dx.doi.org/10.1016/0278-4343(93)90058-6.

9

Varisco, M., Cochia, P., Góngora, M.E., Bovcon, N., Balzi, P., Vinuesa, J., 2017. Bycatch of the Southern King Crab (Lithodes santolla) in the Patagonian shrimp fishery in the Southwestern Atlantic Ocean. Can it contribute to the depletion of its population? Ocean & Coastal Management 136, 177–184. Wilson, K., Hardy, I.C.W., 2002. Statistical analysis of sex ratios: An introduction. In: Hardy, I.C.W. (Ed.), Sex Ratios: Concepts and Research Methods. Cambridge University Press, Cambridge, United Kingdom, pp. 48–92, http://C: /Users/Sony/Downloads/Sex_ratios_Concepts_{and}_research_methods.pdf. Yodzis, 2001. Must top predators be culled for the sake of fisheries? Trends Ecol. Evolut. 16 (2), 78–84. http://dx.doi.org/10.1016/S0169-5347(00)02062-0. Zacharia, P.U., Krishnakumar, P.K., Durgekar, N., Raveendra, Anoop, A.K., Muthiah, C., 2006. Assessment of bycatch and discards associated with bottom trawling along Karnataka coast, India. In: Proceedings of the International Symposium on Improved Sustainability of Fish Production Systems and Appropriate Technologies for Utilization Cochin, vol. 1, pp. 434–445. Zairion, A., Hakim, A., Mashar, A., Fahrudin, A., Adrianto, L., Widigdo, B., Y., Wardiatno., 2018. Diversity and distribution of Dorippid Crabs (Brachyura: Dorippidae) in East Coast of Lampung, Indonesia. Environ. Earth Sci. 012056. http://dx.doi.org/10.1088/1755-1315/149/1/012056. Zar, J.H., 1999. Biostatistical Analysis, fourth ed. Upper Saddle River Prentice Hall, 560p. Zhou, Y., Yimin, Y., 1996. Estimation of discards and bycatch in Chinese fisheries. In: Clucas, I.J., James, D. (Eds.), Report on the Technical Consultation on Reduction of Wastage in Fisheries. Tokyo, Japan, 28 October - 1 November 1996 FAO Fisheries Report. No 547 supplement. Rome, FAO, 1996.