Research 241 (2021) 105988

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Fisheries Research

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Fish and spearfisher traits contributing to catch composition

Moys´es C. Barbosa a,*, Osmar J. Luiz b, Cesar A.M.M. Cordeiro a,c, Vinicius J. Giglio a,d, Carlos E. L. Ferreira a a Systems Ecology and Conservation Lab, Department of , Universidade Federal Fluminense, Niteroi,´ 24020141, Brazil b Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, c Programa de Pos-Graduaç´ ao˜ em Ecologia, Universidade Federal do Rio de Janeiro, 68020, Rio de Janeiro, RJ, Brazil d Laboratorio´ de Ecologia e Conservaçao˜ Marinha, Instituto do Mar, Universidade Federal de Sao˜ Paulo, Santos, Brazil

ARTICLE INFO ABSTRACT

Handled by Niels Madsen Spearfishingis a popular activity practiced for recreation and subsistence along the tropical and subtropical of Brazil. Although being an economically important activity, the influence of species traits driving target Keywords: preferences among recreational spearfishers have been poorly explored. is highly selective towards Recreational large trophy species, therefore its effects on top predators, which are generally threatened, have been widely reported as detrimental. Here we test if species traits are useful to predict spearfishers’ target preferences and the Coastal zone management relationship between spearfishers’ experience with catch’s size and composition in a subtropical Brazilian rocky Biological impacts reef. Large macrocarnivores species and species that form schools associated with the pelagic habitat are pre­ Human ecology dicted to form the core of target preferences by spearfishers. More experienced spearfishers captured larger than less experienced ones. Herbivores and macro-carnivorous were the most important trophic groups contributing to catch composition , being parrotfishes (Scarinae) the most selected. Spearfishers with more years of practice acknowledged that stocks of many targeted species have been depleted. Spearfishersclaim that spearfishing is sustainable because their catches are selectively captured, but such selectivity is highly dependent on fisher experience, frequency and body size of available targets. Most importantly, spearfishing is highly selective for large and vulnerable individuals, especially big old fat fecund females, which are the in­ dividuals that need to be protected most. There is an urgent need to control species identity and size of captures to avoid stocks colapse and local functional extinctions.

1. Introduction is a popular sport and social activity, involving several methods (e.g. boat-fishing,shore-fishing and spearfishing),high Fishing is arguably one of the oldest and most pressing anthropo­ levels of fishing effort, and estimated to be practiced by 11.5 % of the genic impacts on marine , with a long history of exploitation world’s population (Griffiths et al., 2010). Recreational landings may by coastal human populations (McCauley et al., 2015; Steneck and even exceed commercial landings in some regions (Schroeder and Love, Pauly, 2019). Overfishing is considered one of the most important 2002), and are largely free from the market or food security anthropogenic impacts on marine , driving severe functional that influence commercial and artisanal fisheries (Brewer et al., 2012). changes (Jackson et al., 2001; MacNeil et al., 2015; Pimiento et al., The same issues that have inflicted concerns in commercial fisheries 2020; Thurstan et al., 2014). Fishing effort is currently exerted over a worldwide (e.g. by-catch, fisheries-induced selection, trophic changes, wide range of habitats, depths and trophic levels (Branch et al., 2010; habitat degradation) are remarkably similar among recreational Sethi et al., 2010). Overfishing is attributed mainly to commercial sectors (Font and Lloret, 2011). fisheries( Pauly et al., 2003), and most studies have focused on that type Among recreational fisheries, spearfishing presents high selectivity of activity. In contrast, research on recreational fisheries is limited, yet on target species, which implies in large proportional impact over they have been increasingly recognized for contributing to the decline of certain taxa (Bejarano et al., 2013). Spearfishers target mainly large vulnerable species such as (Coleman et al., 2004; Cooke and body-sized species, including top and meso predators (Guabiroba et al., Cowx, 2004; Guabiroba et al., 2020) and (Young et al., 2014). 2020; Lloret et al., 2008; Nunes et al., 2012), and impacting less the

* Corresponding author. E-mail address: [email protected] (M.C. Barbosa). https://doi.org/10.1016/j.fishres.2021.105988 Received 10 August 2020; Received in revised form 15 April 2021; Accepted 23 April 2021 0165-7836/© 2021 Elsevier B.V. All rights reserved. M.C. Barbosa et al. Fisheries Research 241 (2021) 105988 non-target species (Frisch et al., 2008; Giglio et al., 2018). However, 2. Methods when the environment is already overexploited, non-target species are heavily caught (Pinheiro and Joyeux, 2015). The impact of the selective 2.1. Study area removal of large predators, such as groupers and snappers, is a major ◦ ◦ ecological problem because they have biological characteristics that The study area is located in Arraial do Cabo (23 58’S–42 00’W), make them susceptible to exploitation even under low fishing effort state of Rio de Janeiro, southeastern Brazil (Fig. 1). For over a century, (Coleman et al., 2000). Sex-change, disproportional sex ratio, late the city has followed its natural vocation as a , with gonadal maturation and longevity are characteristics that are associated approximately 30,000 residents and 1340 active fishers.In 1997 a local with population decline even at low levels of exploitation (Sadovy de marine partially-protected area named, Arraial do Cabo Marine Mitcheson et al., 2013). Because fecundity is correlated with body size, Extractive Reserve (ACMER) was implemented. In the ACMER, only the removal of the largest individuals decreases the reproductive po­ local fishersare allowed to fish.Fishing regulations are poorly enforced, tential of populations (Alonzo et al., 2008; Barneche et al., 2018; Pauly resulting in a typical overexploitation scenario (Bender et al., 2014; et al., 2002). This selective removal of large predators can have a Giglio et al., 2017). The fishinggears used by the local traditional fishers top-down effect on , distort food webs, alter ecosystem are hook and line, gillnet, beach seine and spearfishing.In recent years, function, increase vulnerability to other disturbances and change the however, recreational fishinghas increased in the region along with the composition of natural communities (Lloret et al., 2008). Spearfishers intense growth of tourism in the region, further increasing the range of also target secondary consumers such as parrotfishes,which are critical exploited species. Today, spearfishing in ACMER is a popular recrea­ primary producer consumers which have important functional roles on tional activity. Spearfishingregulations require a fishinglicense both for reef systems (Cinner et al., 2009; Hughes et al., 2007). These effects recreational and professional fishers. The former allows a maximum caused by the removal of key species lead to destabilizing fish pop­ daily catch of 15 kg per spearfisher, plus a large fish of any size. The ulations in reefs environments where spearfishing is more intense latter, does not include catching limits and allows the commercialization (Venturelli et al., 2009). of the catch. All spearfishers (recreational or professional) must follow In the Brazilian coast, recreational spearfishingis a popular activity size limits for certain species (Freire et al., 2012). practiced along of the coast and inland , but its effects on fish Unfortunately, catch limits and license holding are not enforced, in communities is poorly documented (Freire et al., 2016). The effects of consequence, illegal fishing occurs, especially at night because the ma­ recreational and artisanal spearfishing over some species have contrib­ jority of recreational spearfishers do not hold fishing licenses. In addi­ uted to species decline, as in the case of the endemic greenbeak par­ tion, regulations prohibit the use of scuba equipment for any rotfish, Scarus trispinosus, which population demography was deeply fishingactivity. However, in ACMER, few local professional spearfishers affected (Roos et al., 2016), leading to local functional extinctions (n = 6) have permission to use hookah (surface-supplied air) and (Bender et al., 2014). Here, we evaluated if species traits predict target commercialize their catch, but this category of spearfishing was not preferences among recreational spearfishers.We combined quantitative included in our study. data from recreational fishing captures with reef fish assemblage as­ sessments and fishers’ characteristics to determine the effect of catch selectivity. This study aiming to inform management of recreational 2.2. Data collection spearfishing inside a marine partially-protected area. To assess fisher’s perception and catch composition, we conducted

Fig. 1. Map of study site and interview locations.

2 M.C. Barbosa et al. Fisheries Research 241 (2021) 105988 face-to-face interviews through semi-structured questionnaires with 132 (Table 1). Data on, maximum total length and schooling behavior were spearfishers, from February 2012 to January 2013. The surveys were obtained from FishBase (Froese and Pauly, 2020) and primary literature. done by boat along the coast of Arraial do Cabo, and in the wharfs and We considered schooling species to be those that regularly form polar­ beaches when the spearfisherreturned from fishing.Overall, 22 fishing ized, cohesive groups of 20 or more individuals. Fish frequency and sites (1–25 m depth) were identifiedamong the spearfishers( Fig. 1), 75 density was assessed through underwater visual census along 591 % accessed the fishing sites from the shore while the remaining 25 % transect lines (20 × 2 m) run parallel to the shore, across 10 represen­ used small motorboats (4–6 m). Interviews were conducted with every tative sites of the study area, at different depths (Floeter et al., 2007). spearfisherfound in the or in land during weekends, twice time a The range of depths surveyed was similar among all sites. We also month and during holidays. For each spearfisherinterviewed, details of verifiedthe relationship among spearfishers’ experience with the species catches (fishspecies and length); main target species; perception about catch, their respective sizes and exploited sites. Also, we enquired the catches (if target species had increased, decreased or unchanged); whether there have been changes in the perception of spearfishersabout fishing effort (time spent in the fishery until moment of interview, plus catch over the years of practice, if they feel that catches had increased, the intent time); years of practice in the activity; fishing frequency decreased or remained unaltered. The research was approved by Sistema (average dives per year). To determine the experience, spearfisherswere de Autorizaçao˜ e Informaçao˜ em Biodiversidade (Sisbio-ICMBio/IBA­ asked about the number of dives conducted per year and number of MA/Brazil nr. 34616). years they had been spearfishing. For instance, a spearfisher who con­ ducting 30 dives a year and with 10 years of practice, the experience 2.4. Data analysis considered was 300 dives. We compared the experience level of spearfishers in relation to tro­ 2.3. Fishing data phic groups of targeted (would like to catch) and caught species (catch observed at the time of interview) through one-way ANOVA. When The average catch body size and abundance of each species captured necessary, the Tukey post-hoc test was performed followed by Spear­ were measured. From the body sizes of the catch, were calcu­ man’s rank correlation, which tested whether the relationship between lated using the length- relationship available in the FishBase mean weight, length, abundance and of the catches with database (Froese and Pauly, 2020). The trophic level of each fishspecies the experience attributed (extrapolated number of dives) to each fisher. was obtained from FishBase database (Froese and Pauly, 2020). The Data was log-transformed to reach assumptions of normality and het­ trophic level expresses a position of an organism within the of erogeneity. Linear regressions were used to determine the relative the local (Pauly et al., 2000) and is based on prey importance of different species-level traits associated with catch items in their diet. The mean trophic levels of spearfishingcatches were composition of spearfishers (Table 1). The relationship of species traits calculated by averaging the trophic levels for the entire catch by weight with the target preferences of spearfishers were investigated using (Lloret et al., 2008). For each species, the index of intrinsic vulnerability generalized linear mixed effect models (GLMMs) assuming a binomial = = that defines the vulnerability of marine fishes to fishing, was obtained distribution for the response variable (non-targeted 0, targeted 1) from FishBase (Froese and Pauly, 2020). It is based on the life-history and a log-link function for the predictors. The models are ranked ac­ and ecological characteristics of each species (Cheung et al., 2005) cording to Akaike information criteria for small sample size (AICc), delta and ranges from 1 to 100 where a higher value represents greater AICc and Akaike weights. We used the delta AICc to select the most vulnerability. The average intrinsic vulnerability index of fish in the likely models, which were those with differences lesser than 8 among catch was calculated from the arithmetic mean of the intrinsic vulner­ the AIC value of the given model and the model with the lowest AIC. The ability index of fish taxa weighted by their catch (Lloret et al., 2008). Akaike weights can be interpreted as the probability that a certain model Furthermore, the International Union for Conservation of Nature (IUCN) is the best among the set of models. Taxonomic family was included as a Red List (IUCN, 2020) and national list of Threatened Species (MMA, random variable to account for the non-independence of species shared 2014) were used to assess the conservation status of all species caught. ancestry. Partitioning of variance to determine the relative importance Averages of capture were done per unit of fishing effort (CPUE) of each explanatory variable in the model was calculated using the R expressed as weight of the catch (biomass) by fishingeffort (fisher/hour package hier.part (Walsh and Mac Nally, 2015). All variables were tested fishing). Fish trophic guilds were assigned to species following the for collinearity prior to analyses using rank order correlation (collin­ = > classification of Ferreira et al. (2004). From the target species cited as earity |r| 0.7; Dormann et al., 2013), except for diet categories that targets in the interviews, we evaluated which characteristics they share were non-ordered). All analyzes were performed on R software, version and which potentially explain their attractiveness for spearfishers. We 3.6.1 (R Development Core Team, 2019). selected traits as maximum total length; schooling behavior; trophic guild, relative abundance of species in the study area and habitat use 3. Results

3.1. Catches composition and fishing effort Table 1 Traits used to calculate functional attributes to catches and targets of spearfishing. A total of 251 fishindividuals from 35 species and 21 families were observed in catches, in which six were pelagic and 29 reef-associated Trait Units References species. Parrotfish species (family Labridae) were the most captured Body Size Total length (cm), continuous (Froese and (n = 47 individuals) and also had the largest contribution in weight with Pauly, 2020) Trophic guild Macrocarnivores, herbivores, invertivores, (Ferreira et al., 19 % of total catch (Table 2). The macrocarnivore comb , Myc­ planktivores and omnivores 2004) teroperca acutirostris, was the species with higher individual contribution Schooling Index from 1 or 2 indicating solitary or (Froese and on weight (23.2 kg) to total catch, followed by the herbivore gray par­ behaviour schooling species Pauly, 2020) rotfish Sparisoma axillare (22.6 kg), and the Agassiz’s parrotfish Spar­ 2 Frequency Number of transects (40 m ) that species was (authors) isoma frondosum, (17.7 kg) (Table 2). Invertivores were the most observed in relation to total of transects, = continuous. abundant trophic group (n 86, 34.2 % of total abundance), followed Density Mean abundance of species in 40 m2, (authors) by macrocarnivores (n = 82, 32.6 %), herbivores (n = 72, 28.6 %) and continuous. omnivores (n = 11, 4.6 %). However, macrocarnivores, followed by Habitat use Benthic, pelagic or reef. (Froese and herbivores, invertivores and omnivores contributed with 44 %, 31 %, 22 Pauly, 2020) % and 6 % of catch, respectively. Trophic level in the catches ranged

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Table 2 Species captured by spearfishers according total weight of each species (W).

Family Species Trophic Guild N IUCN category MMA category TL IV L ± SE (cm) W (kg) % TW

Epinephelidae Mycteroperca acutirostris MACAR 17 LC NE 3.4 58 41.9 ± 2.8 23.19 13.24 Labridae Sparisoma axillare HERB 27 DD VU 2 38 33.0 ± 1.7 22.60 12.91 Labridae Sparisoma frondosum HERB 18 DD VU 2 29 29.1 ± 1.6 17.71 10.11 Carangidae Seriola dumerili MACAR 19 LC NE 4.5 54 32.4 ± 2.2 16.37 9.35 Scombridae Euthynnus alletteratus MACAR 10 LC NE 4.5 57 40.6 ± 8.1 11.56 6.60 Carangidae Trachinotus falcatus INV 8 LC NE 4 42 35.9 ± 2.7 10.63 6.07 Mugilidae Mugil curema OMN 12 LC NE 2 59 32.2 ± 2.5 10.27 5.86 Epinephilidae MACAR 15 VU VU 4.4 72 34.0 ± 1.4 8.66 4.94 Priacanthidae Priacanthus arenatus INV 30 LC NE 4 25 25.1 ± 1.3 8.57 4.90 Holocentridae Holocentrus adscensionis INV 28 LC NE 3.1 35 22.9 ± 1.1 7.92 4.52 Muraenidae Gymnothorax moringa MACAR 2 LC NE 4.5 85 115.0 ± 0.0 7.50 4.28 Haemulidae Anisotremus virginicus INV 7 LC NE 3.6 37 26.1 ± 4.1 4.97 2.84 Kyphosidae Kyphosus sectatrix HERB 9 LC NE 2 56 27.1 ± 2.5 4.51 2.57 Carangidae Seriola rivoliana MACAR 7 LC NE 4.5 76 32.3 ± 1.9 4.27 2.44 Haemulidae Anisotremus surinamensis INV 1 DD NE 3.6 56 50.0 ± 0.0 3.03 1.73 Monacanthidae Aluterus monoceros INV 3 LC NE 3.8 48 31.8 ± 10.6 2.80 1.60 Narcinidae Narcine brasiliensis MACAR 3 DD NE 3.2 35 46.0 ± 6.2 2.66 1.52 Sparidae Diplodus argenteus OMN 6 LC NE 3.1 45 20.5 ± 1.9 2.20 1.25 Acanthuridae Acanthurus chirurgus HERB 5 LC NE 2.1 23 24.6 ± 2.1 1.80 1.03 Centropomidae Centropomus parallelus MACAR 1 LC NE 4.2 55 40.0 ± 0.0 0.66 0.38 Carangidae Caranx crysos MACAR 2 LC NE 4.1 34 27.0 ± 0.0 0.58 0.33 Carangidae Caranx hippos MACAR 1 LC NE 3.6 41 32.5 ± 0.0 0.49 0.28 Sparidae Archosargus rhomboidalis OMN 1 LC NE 2.9 36 22.0 ± 0.0 0.43 0.24 Labridae Halichoeres brasiliensis INV 1 DD NE 3.7 52 26.6 ± 0.0 0.32 0.18 Carangidae Seriola lalandi MACAR 3 LC NE 4.2 69 17.1 ± 1.3 0.24 0.14 Acanthuridae Acanthurus coeruleus HERB 1 LC NE 2.2 59 19.0 ± 0.0 0.21 0.12 Dactylopteridae Dactylopterus volitans INV 3 LC NE 3.7 31 18.7 ± 1.8 0.20 0.12 Haemulidae Orthopristis ruber INV 1 LC NE 3.6 33 24.4 ± 0.0 0.19 0.11 Monacanthidae Stephanolepis hispidus OMN 3 LC NE 2.6 30 14.2 ± 2.1 0.17 0.10 Labridae Sparisoma radians HERB 2 LC NE 2 14 14.0 ± 0.0 0.11 0.06 Mullidae Pseudupeneus maculatus INV 1 LC NE 3.7 35 15.0 ± 0.0 0.08 0.04 Lutjanidae Lutjanus jocu MACAR 1 DD NE 4.4 66 15.0 ± 0.0 0.07 0.04 Gerreidae Diapterus rhombeus INV 1 LC NE 3 18 13.3 ± 0.0 0.06 0.03 Sparidae Pagrus pagrus MACAR 1 LC NE 3.9 66 15.0 ± 0.0 0.05 0.03 Chaetondotidae Chaetodon striatus INV 1 LC NE 3.5 12 10.5 ± 0.0 0.04 0.02 TOTAL 251 175.12

Trophic Group: MACAR = macrocarnivores, INV = invertivores, HERB = herbivores and OMN = omnivores; N = total number of individuals; IUCN vulnerability categories: LC = least concern, DD = data deficientand VU = vulnerable; MMA vulnerability categories: NE = not evaluated and VU = vulnerable; TL = trophic level; IV = intrinsic vulnerability, L ± SE = mean length and standard error and %TW = relative weight caught. from 2 (Sparisoma axillare and others herbivorous species) to 4.5 frequency of occurrence (Table 4). (Euthynnus alletteratus and others macrocarnivorous species). The mean trophic level in the spearfishers catch was 3.44. The mean intrinsic 3.3. Spearfisher profile vulnerability to fishing of the fish species caught by spearfishers in Arraial do Cabo was moderate (46.5), ranging from low (Chaetodon All fishersinterviewed were male with age varying between 15 and striatus = 12) to very high (Gymnothorax moringa = 85) (Table 2). 62 years (average = 34 ± 0.8 years). The years of practice in spearf­ Furthermore, 16 % of the species caught by spearfishers had highly to ishing ranged from first-time attempters to > 44 years practicing very highly vulnerable level to fishingpressure. About the conservation spearfishing (average = 10 ± 10.3). The annual frequency of spearf­ status, only Epinephelus marginatus is listed at global and national level ishing varied between 1–240 days per year (average 33 ± 3.7 days). The (IUCN, 2020 and MMA, 2014), while two species of parrotfish (Spar­ experience ranged from 1 to 4400 dives of practice isoma frondosum and S. axillare) are listed as vulnerable in the national 1 (average = 421.4 ± 73.1). Only 18 % of respondents were considered as list (MMA, 2014). The CPUE (kg.spearfisher.hour of fishing ) varied local residents. The experience influencedsignificantly the composition between 0 and 7.1, with a mean value of 0.98 ± 0.15 (± standard error). of trophic group targets (ANOVA, F4,399 = 10.20, p < 0.001) and catches of the fisheries (ANOVA, F4,265 = 17.16, p < 0.001) (Fig. 3). The more 3.2. Traits analysis experienced spearfishers(i.e. with more dives of practice) preferentially targeted macrocarnivores, while less experienced were less selective, Trait analysis of catches (GLMM) indicated that species targeted by seeking herbivores, invertivores, omnivorous or had no specific target spearfishers tend to be larger, common, form schools, make use of the (Fig. 3A). The catch showed similar tendencies of the aim focus of pelagic realm and have a macrocarnivorous diet (Fig. 2a, Table 3). The fishery (Fig. 3B). Body size (r2 = 0,17) and weight (r2 = 0,15) were ‘habitat’, ‘macrocarnivores’ and ‘planktivores’ have extremely large predictive of spearfishers with greater experience (p < 0,001) (Fig. 4). confidence intervals encompassing the significance threshold level. However, only body size is considered in the multivariate model because However, we decided to keep these variables because of their large effect of the high correlation between those variables (r = 0.85). Both corre­ sizes, as supported by the model selection procedure (Table 3). Density lations are indicated in Fig. 4 but the weight relationship is shown only of individuals in visual census was not retained as influentialvariables in for reference. the finalmodel, and only planktivorous species were commonly avoided Spearfishers’ perceptions regarding temporal changes of target spe­ by spearfishers (Fig. 2b). The habitat type and trophic guild were the cies’ abundance were directly associated to years of practice (ANOVA, most important predictors of target species, explaining > 50 % of total F2, 117 = 9.51, p < 0.05) (Fig. 5). Seventy-nine percent of spearfishers variance, followed by schooling behavior, maximum length and the with an average experience of 13 years reported that abundance of

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Fig. 2. Relationships of fish species traits (a) and trophic guilds categories (b) with the likelihood of being targeted by spearfisher. Values plotted are model odds ratios (OR; points) with 95 % confidenceintervals (CIs; solid horizontal lines). Where CIs do not encompass 1 (vertical dashed line), the trait was significantlymore likely (OR > 1) or less likely (OR < 1) be targeted.

Table 3 Model selection based on information criteria analysis for the generalized linear mixed-effect model for association between species-level traits of fishes and target preferences by spearfishers. The selected ‘best’ model in indicated in bold.

Variables in the model Log-likelihood AICc Delta AICc Akaike weight

Body size þ frequency þ schooling þ habitat þ trophic 36.675 95.1 0.00 0.781 Body size + frequency + schooling + habitat + trophic + density 37.073 98.3 3.16 0.161 Body size + frequency + schooling + habitat + density 43.882 102.6 7.54 0.018 Frequency + schooling + habitat + trophic 45.115 102.9 7.78 0.016 Frequency + schooling + habitat + trophic + density 41.827 103.1 7.98 0.014

targeted species declined, while 19 % with an experience average 5.5 Table 4 years believe that abundance has not changed. Only 2 % subjects with Resume of the final generalized linear mixed effect model for the association experience average of three years believe that stocks increased between species-level traits of reef fishesand target preference by spearfishersin throughout his experience in the activity (Fig. 5). Arraial do Cabo as the response variable. Parameters are coefficientestimates of fixedvariables, standard error (s.e.), test statistic (z-value), probability (p-value) and the independent effect (IE) of each explanatory variable (%) on the response 4. Discussion variable, calculated by hierarchical partitioning. Reference levels for this regression were set as ‘no’ for schooling behavior; as ‘pelagic’ for habitat type, Our study on the subtropical reefs of southeastern Brazilian coast and as ‘macrocarnivores’ for trophic guild. revealed that biological and demographic attributes were useful to Variable estimate s.e. z-value p-value IE (%) predict the preferred species captured by local spearfishers.Spearfishing is among the most selective fishing gear, the spearfishers identify their Intercept 19.630 8.1 × 102 0.024 0.980 Body size 3.229 1.300 2.484 0.012 20.29 target visually and are able to single out individuals for capturing. The Frequency 2.341 0.856 2.735 0.006 5.25 chosen prey is based both on the hunter requirements and on what is Schooling behaviour 6.976 3.123 2.234 0.025 20.75 available in the environment, preferentially at this sequence. Maximum Habitat type (reef) 23.840 810.0 0.029 0.976 26.86 body length, habitat type, diet, frequency of occurrence and schooling Trophic guild 26.82 behavior were the traits that most influence the likelihood of being invertivores 5.094 3.590 1.419 0.155 omnivores 3.845 5.388 0.714 0.475 targeted by recreational spearfishers. The maximum body length was planktivores 192.7 2.2 × 107 0.000 0.999 the most important attribute associated with captures. Large species that herbivores 0.302 4.553 0.066 0.947 generally occupy higher trophic levels (top predators) have great value as food and acceptance to popular taste. Large fishesare, or at least, give

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Fig. 3. Relationship of mean (±SD) experience of spearfishers(number of dives) with A: trophic guild target of fisheries,and B: trophic guild catches. Letters above bars indicate statistically significant differences (p < 0.05). (MACAR: Macrocarnivores; INV: Invertivores HERB: Herbivores; NP: No Preference; NF: No Fishes; NA: not available (catch could not be inspected). ANOVA: Target (F-value = 10.2, p < 0.001), Captured (F-value = 17.2 p < 0.001).

Fig. 4. Non-parametric Spearman rank correlation of catch indicators and spearfisher experience (number of dives). the impression of being challenging to be caught and this is an important populations to recover from overfishing (Birkeland and Dayton, 2005; component of the spearfishers’ psyche (Nunes et al., 2012). As expected, Coleman et al., 2004). In Brazil and elsewhere, large-bodied reef fishes large fishes are heavily targeted in fisheries and tend to suffer greater were already reported to be disproportionately threatened in relation to declines than small-sized fishes (Dulvy et al., 2000; Stevens, 2000). other body size categories (Bender et al., 2013; Luiz et al., 2016). Commonly, large top predators accumulate life attributes (e.g. high Our result that large sized carnivores are selected as target species by longevity, sex-ratio and late maturation) that make them especially spearfishers in SE Brazil confirms the observation that groupers and vulnerable to exploitation, often leading to population collapse and snappers are very sought after by spearfishers elsewhere (Giglio et al., extinction (Bender et al., 2013). More critical, larger individuals usually 2020; Pinheiro and Joyeux, 2015). We have also identified have exponential greater fecundity (Barneche et al., 2018; Birkeland and pelagic-associated shoaling species (e.g. Seriola dumerili and Euthynnus Dayton, 2005). Altogether, these characteristics make the selective alletteratus) as highly prized targets at our study site. The selection for removal of large specimens, even at low fishingeffort, more difficultfor these traits are probably site-specific, being more common in offshore

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in overexploited environments, decreasing selectivity. The facility to find and harvest the resource often allows a decrease in selectivity for less-expert spearfishersand the maintenance of high numerical yields in over-exploited areas (Pinheiro and Joyeux, 2015). The mean trophic level of the catch in our study was greater than the mean level of catches in the (3.24; Martín-Sosa, 2019), lower than in Cape Creus, Spain (3.89; Lloret et al., 2008) and similar to mean level of catches in the Azores Islands (3.40; Diogo and Pereira, 2014). The lower average in our study compared to Cape Creus, can be partly explained by the presence of abundant herbivore species (e.g. S. axillare and S. frondosum), with low trophic levels that are important targets for all spearfisher levels. However, even in overexploited reefs recreational fishing still removing less abundant fish with high trophic levels. The average intrinsic vulnerability in the spearfishingcaught (46.05 out of 100) is moderate (Cheung et al., 2007). This value is low compared to average vulnerability of spearfishing catches at temperate reefs of the Cape Creus in Spain (54.15; Lloret et al., 2008), for example, but similar to catches of spearfishers at Canary Island (45.72; Martín-­ Sosa, 2019) and novice spearfishersat Sao˜ Miguel Island in Azores (3.3; Diogo et al., 2017). Although the average vulnerability index among Fig. 5. Relationship of mean (+ SD) years practice of spearfishers with catches was not high, three protogynous species classifiedas vulnerable perception about the currently catches, letters above bars indicates statistically (IUCN, 2020 and MMA, 2014) were common. The average caught size of significant differences (p < 0.05). the protogynous species Epinephelus marginatus (34 cm) is far below its L50 size (47 cm, Andrade et al., 2003). Sex-changing species are more islands and coastal sites with short shelf platforms (Diogo et al., 2017; vulnerable to overexploitation because selective fishingpressure affects Guabiroba et al., 2020; Young et al., 2015). Most pelagics that occur in sex ratio (Armsworth, 2001; Hawkins and Roberts, 2003). The removal the study region are targeted mainly because they are large. A study in of large individuals by spearfishingcan adversely affect the reproductive the tropical reefs of northeastern Brazil, where the potential of these vulnerable species (Lloret et al., 2008). Larger in­ break is very short (~5 miles in some places), also detected high catches dividuals are proportionally more fecund, having bigger and more eggs of pelagic species (Nunes et al., 2012). Another study in southeastern while producing larvae with better survival rates (Hixon et al., 2014). subtropical reefs where the continental shelf break is located ~200 miles Even a low fishing effort over sequential hermaphrodites such as away found high catches of demersal fishes (Pinheiro and Joyeux, E. marginatus, can significant affect the spawning success of the popu­ 2015). In Arraial do Cabo there is a strong oceanic influencebecause of lation (Lloret et al., 2008). As being also a sex-change group, fishing the coastal morphology and events close to shore, conse­ could impose strong selective on parrotfishes, favoring in­ quently increasing the occurrence of pelagic species. It seems that spe­ dividuals to change sex earlier (Hawkins and Roberts, 2003). Terminal cificregional coastal configurationscontribute to fishspecies occurrence phase of the large species as S. axillare and S. frondosum are becoming and captures. rare in the region as spearfishingpressure increase (Bender et al., 2014; Aspects of the behavior of fishes, such as schooling and spawning Cordeiro et al., 2016). Large species as Scarus trispinosus, already aggregations, are commonly reported to increase fishing success considered functional extinct in Arraial do Cabo due to spearfishing, (Januchowski-Hartley et al., 2012). Schooling behavior was also an present typical life history traits, as late maturity and long lifespans, that important predictor that explains target preference by spearfishers. make than high vulnerable to intense fishing (Roos et al., 2020). Large School-forming fishes attract more attention from spearfishers, as they individuals have different functional role and fishing pressure over look more abundant and may represent an easier target that are harder parrotfish can drastically reduce grazing rates, affecting critical func­ to miss than solitary species. School forming species in our study site tions on reefs (Skinner et al., 2019). include some semi-pelagic species that are heavily overfished, like ca­ Catch composition and capture success rate are suggested to vary rangids and scombrids, but also include nominally herbivorous reef according to spearfishers’ experience, fishassemblage composition and fishes that attain large body sizes, such as parrotfishes (Sparisoma spp. ecosystem health (Diogo et al., 2017). Although our study showed a and Scarus spp.) and chubs (Kyphosus spp.). The former two genera of direct relationship between the spearfishers experience and the species parrotfishes have been intensely overfished in the last decades (Bender caught, the fish abundance and the trophic level of species caught et al., 2014), resulting in the largest species of this group being cate­ cannot be associated exclusively with experience. Less experienced gorized into threatened categories (MMA, 2014). Despite attaining large spearfishersare less selective and can shoot at any fish,especially those sizes, sea chubs are not targeted by experienced spearfishers, as they visually more abundant. In a study investigating the effects of different consider them of having bad taste, although naïve spearfishers levels of experience, Giglio et al. (2018) verifiedthat novice spearfishers frequently see these fishesas a target. Yet, some abundant species such did not specify a target species or family, while most intermediate and as big eyes, Priacanthus arenatus, although not large, are found forming experienced spearfishers targeted mainly mesopredators. The capture large schools, being an easy target for spear. success rates and species composition vary among spearfisherdepending As expected, the frequency of a fish species in census samples is a on their experience and the targeted habitat (Assis et al., 2018; Lincoln good predictor for spearfishing captures. Locally common species are Smith et al., 1989). In general, experienced spearfishers were better readily available to be captured. However, even being abundant is not equipped, explore different areas, dive deeper and further offshore, and enough to be a target, thus the fishneed additional attributes to became are more selective regarding fish size and target species (Diogo et al., a preferred target. Species frequency on the reef can cause fisher to 2017). Both the less experienced and less selective fishersand the more reduce selectivity to maintain high abundance in catches (Lincoln Smith experienced, more selective fisher,can contribute to the unsustainability et al., 1989). Pinheiro and Joyeux (2015), working with recreational of the activity in already degraded places (Pinheiro and Joyeux, 2015). fishingon two Brazilian reefs in the southeastern, compared a preserved This comparative analysis between beginners and expert fishers in­ and an overexploited reef and found that catch change to multi-specific dicates how difficultis to generalize about the selectivity characteristics

7 M.C. Barbosa et al. Fisheries Research 241 (2021) 105988 and the biological impacts of the recreational spearfishing,because each minimize the effects of spearfishingon target species, and to enhance the level of experience has different levels of selectivity. Although spear­ protection of functionally important species. Inside MPAs, managers can fishersoften claim this method as highly selective and supposedly of low adjust controls for catches, establish a minimum and maximum size of impact, they ignore the learning curve effect, which makes non-selective capture for the main species caught, including the unmatured in­ beginners to cause large impacts. Furthermore, most of the spearfishers dividuals. These strategies need to include a maximum daily catch, with generally do not have the knowledge about species life cycle and the a ban caught of locally overfished species, including functional impor­ impacts over sex-changing species and specially the disproportional tant herbivorous fishes,like parrotfishesand species with high status of importance of big old fat fecund females (BOFFFs) (Hixon et al., 2014). threat. In French MPAs, for example, groupers (E. marginatus) are not Since experienced spearfishers recognize a decreasing tendency in allowed to be caught by spearfishers( Font et al., 2012). In , as in target species throughout the years, while least experienced do not, the Gulf of , several species with different status of threat cannot characterize a classical indicative of overfishing (Bunce et al., 2008; be caught by spearfishing( FWC, 2020). Also, it is necessary to establish McClenachan, 2009; Pinnegar and Engelhard, 2008). Studies have re­ a restrictive management for BOFFFs, which is well known to function as ported a multi-decadal decrease of targeted fishspecies by spearfishing the most important breading stocks (Barneche et al., 2018; Birkeland in Arraial do Cabo (Bender et al., 2014; Giglio et al., 2020). In the same and Dayton, 2005; Hixon et al., 2014). Local no-take areas need to be way, more experienced commercial fishers acknowledge greater de­ implemented in critical habitats and in sites supported by fishers local creases on species abundance and body size. Environmental changes and ecological knowledge (Bender et al., 2014). Additionally, it is necessary lack of baselines for marine ecosystems have profound implications in to ensure that informative material about these rules are promptly our perceptions of what is a natural environment (Lotze and Worm, available for spearfishers.All these management initiatives together can 2009; Knowlton and Jackson, 2008). The difficulty of people in help reduce the impacts of recreational spearfishing, while educating perceiving environmental modificationsis because each generation sets practitioners about the effects of fishing. their own baseline of stock size and species composition based on the beginning of their experiences, using this to evaluate changes (Pauly, CRediT authorship contribution statement 1995). As generations change, the perception of environmental base­ lines become increasingly shifted, misinforming fisheries management. Moyses´ C. Barbosa: Conceptualization, Formal analysis, Writing - For a long time, recreational fishing had been considered less original draft, Writing - review & editing. Osmar J. Luiz: Formal harmful for marine biodiversity than , based on ev­ analysis, Writing - original draft, Writing - review & editing. Cesar A.M. idences of comparable reported effort (Coleman et al., 2004). However, M. Cordeiro: Formal analysis, Writing - original draft, Writing - review the growing human occupation at coastlines and continuous people & editing. Vinicius J. Giglio: Formal analysis, Writing - original draft, engagement on recreational fishing had changed this scenario to an Writing - review & editing. Carlos E.L. Ferreira: Formal analysis, activity with recognized deleterious effects worldwide (Cooke and Writing - original draft, Writing - review & editing. Cowx, 2004). Spearfishing critically impacts large and longevous spe­ cies, especially those on the top of food webs (Gerhardinger et al., 2006; Declaration of Competing Interest Giglio et al., 2017), and species that perform important ecological functions for the reef ecosystem, such as parrotfishes (Bender et al., The authors report no declarations of interest. 2014; Freitas et al., 2019). Spearfishingis a highly selective activity, but selectivity is not equal to sustainability as the majority of spearfishing Acknowledgements advocates claim. However this is still the only fishingmodality in which the fishercan choose precisely the prey that will be captured (Coll et al., M.C.B. acknowledges the Coordenaçao˜ de Aperfeiçoamento de Pes­ 2004). If there is proper information and updated guidance on what soal de Nível Superior (CAPES – Finance Code 001), Costao˜ Rochoso species, sizes and quotas to be captured, the activity certainly can be project (FUNBIO under the grant Pesquisa Marinha 020/2017) and more sustainable (Font et al., 2012). However, as a recent report make Ecohub for financial support. We would like to thank all spearfishers evident that more than 90 % of the in Brazil have no infor­ who participated in the survey and Carlos Barboza for the analysis and mation on catches and landings (Zamboni et al., 2020), the efforts to comments. ICMBio and RESEXMar for local support. C.E.L.F. is lead recreational fishing as being less environmentally degrading, are continuing granted by CNPq and FAPERJ. V.J.G. received a postdoctoral pending over local government initiatives. grant #2017/22273-0, Sao˜ Paulo Research Foundation (FAPESP). We We observed higher catches of herbivores and macrocarnivores thank H. Pinheiro and an anonymous reviewer whose comments helped species. The predator-prey relationship is important to the ecological improve the manuscript. balance of these communities and the removal of predatory fish can affect the entire reef community structure (Floeter et al., 2006). References Removing some species and individuals faster than others can lead to distorted food webs, altered ecosystem function, and increased vulner­ Alonzo, S.H., Ish, T., Key, M., MacCall, A.D., Mangel, M., 2008. The importance of incorporating protogynous sex change into stock assessments. Bull. Mar. 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