Spatial variation of parrotfish assemblages at oceanic islands in the western Caribbean: evidence of indirect effects of fishing?

Introduction

Local stressors such as overfishing have caused significant changes in the structure and function of coral reefs (Jackson et al., 2001; McLean et al., 2016). Overexploited fisheries tend to shift towards lower trophic levels (Taylor, 2014), with growing captures of smaller and less commercial species, usually herbivores (Burke et al., 2011). The assessment of herbivores populations in coral reefs subject to fishing activities is compulsory, yet the lack of rigorous data on fishing effort remains one of the main obstacles to understanding fishing effects (Stewart et al., 2010). Therefore, to assess populations in localities with poorly documented coastal fishing efforts, it is necessary to resort to additional information linked to such efforts.

Different measures, such as human population density, have been proposed to indicate fishing effort (Stewart et al., 2010). There are two ways in which human density can affect fish populations locally (Williams et al., 2008). Directly, through overfishing, with a selective effect on targeted species, and indirectly, through habitat degradation, with a more widespread effect on both targeted and non-targeted species (Pauly, 1990; Williams et al., 2008; Stewart et al., 2010). Studies in insular territories around the world have shown a negative relationship between human population density and biomass and abundance of fish populations in coral reefs adjacent to inhabited territories (Clua & Legendre, 2008; Williams et al., 2008; Bellwood, Hoey & Hughes, 2012). Related information such as access to local markets and urbanization are also reliable indicators to approach the fishing pressure level of a particular locality (Aswani & Sabetian, 2009; Brewer et al., 2012, 2013; Cinner et al., 2013). In addition, different biological attributes in fish populations are also proposed as features to study fishing effects.

Individual body size is one of the most operational features to evaluate the effects of overfishing (Rochet & Trenkel, 2003). However, size-based analyses have typically examined assemblage-level patterns of the entire reef fish communities (Jennings et al., 2002; Dulvy et al., 2004; Graham et al., 2005), ignoring possible variation within groups of fishes. In the Caribbean, size-based studies have shown a turnover of fisheries towards species of lower trophic levels, such as parrotfishes (Hawkins & Roberts, 2004; Hardt, 2009; Vallès & Oxenford, 2014) and a size-based study conducted on this group can add resolution to the existing literature on this topic.

Parrotfishes (Labridae: Scarinae) and surgeon fishes (Acanthuridae) are two of the main herbivore clades in coral reefs of the Caribbean (Mumby et al., 2006). Former studies in the Caribbean have linked patterns of spatial variation in parrotfish communities with overfishing. Those studies found a negative relationship between fishing pressure and biomass of large-bodied species and with the individual body weight of all parrotfish species (Hawkins & Roberts, 2004; Vallès & Oxenford, 2014; Vallès, Gill & Oxenford, 2015). Overfishing has also been associated with indirect effects on fish communities through compensatory increases of small species when the larger ones decrease (Dulvy et al., 2004). However, there is scarce evidence of this effect in parrotfish communities. A largescale study by Hawkins & Roberts (2003) found that the abundance of the small-bodied Sparisoma atomarium increased with fishing pressure. Vallès, Gill & Oxenford (2015) found that at higher fishing pressure, Scarus iseri and Scarus vetula were still more and less abundant, suggesting a possible event of competitive release between the two species, but no significant differences supported such hypothesis. Therefore, it is relevant to provide a better characterization of parrotfish spatial variation to explore emergent exploitation impacts within fisheries, especially in small-scale spatial gradient of fishing pressure and in areas where these effects are still unknown.

Furthermore, parrotfishes are an interesting group to assess fishing effects on sex ratios and body sizes of protogynous species, the most common form of sequential hermaphroditism of reef fishes (Gemmell et al., 2019), an issue than remains poorly examined (Buxton, 1993; Coleman, Koenig & Collins, 1996; McGovern et al., 1998; Hawkins & Roberts, 2003; O’Farrell et al., 2016). In Bonaire, abundances of males of S. vetula, Sparisoma viride, Sparisoma aurofrenatum and Scarus taeniopterus increased after a fishing ban (O’Farrell et al., 2016). Likewise, most parrotfish species evaluated by Hawkins & Roberts (2003) showed a decreased in body sizes of males and females with fewer males at higher fishing pressure. In marine protected areas, the authors also found an increase in time of body sizes of males and females of most species. Hence, adding resolution to these relationships is pertinent to monitor their populations over time.

In this study, we used diver-operated stereo-video to assess parrotfish populations and explore the effects of fishing pressure in oceanic islands of the Colombian Caribbean. The stereo-video technique allowed us to gather high-resolution body-length data for a size-based analysis under a qualitative fishing pressure gradient in which we included the best available local information. We anticipated that fishing exploitation would reduce the abundance and average body size of medium and large-bodied species, with a minor contribution of those species to the overall parrotfish biomass. Consequently, small-sized species would have a greater contribution to the overall parrotfish biomass either by having greater abundances at higher fishing pressure or mainly because of the lower contribution of the medium and large-bodied species proportions.

Materials and Methods

Sampling sites and fishing pressure gradient

The Seaflower Biosphere Reserve (SBR) is a complex of islands, atolls, cays, and shoals in the Colombian Caribbean, including one of the largest Caribbean coral reefs complexes (Abril-Howard et al., 2012a) and over 77% of the coral formations of the country (Abril-Howard et al., 2012b). We recorded parrotfish species in coral reef areas of several islands of the SBR: San Andrés (SA), Bolívar Cay (BOL), Albuquerque Cay (ALB), and Providencia and Santa Catalina (PRO). The main island of the archipelago is SA, located 90 km south of PRO, the other inhabited populated island, while BOL and ALB are two small uninhabited cays, 25 and 37 km south of SA, respectively (Fig. 1).

Considering the selectivity of fisheries for large fishes (O’Farrell et al., 2016), metrics such as individual body size, sex ratio, and overall proportions of parrotfishes would reflect different responses to exploitation by comparing them across a fishing gradient (Rochet & Trenkel, 2003; Dulvy et al., 2004). However, at the SBR, no standardized information precludes us to quantify fishing pressure. Therefore, we considered additional drivers based on the literature of the topic (Clua & Legendre, 2008; Williams et al., 2008; Aswani & Sabetian, 2009; Bellwood, Hoey & Hughes, 2012; Brewer et al., 2012, 2013; Cinner et al., 2013). To include species with different levels of interest for the fisheries, we evaluated eleven species of parrotfish across a wide range of body sizes along the established human pressure gradient. We separated the species into three categories: small-sized ones (maximum total length <30 cm) including S. taeniopterus, S. iseri, S. aurofrenatum and S. atomarium; medium-sized species (maximum total length >30–<70 cm) Sparisoma chrysopterum and Sparisoma rubripinne, in addition to S. vetula and S. viride. The large-bodied species (maximum total length >70 cm) included Scarus coelestinus, Scarus coeruleus, and Scarus guacamaia.

The proposed ranking of localities from highest to lowest fishing pressure was: SA, BOL, ALB, and PRO. This order was based on: (1) Human population density (number of inhabitants per square kilometer of reef structure) in SA is 784 inhabitants/km², while in PRO is 18 inhabitants/km² (Gamboa et al., 2012; DANE, 2016; Cámara de Comercio de San Andrés, Providencia y Santa Catalina, 2018). Bolívar and Albuquerque cays have no human population besides a dozen Colombian soldiers; however, fishers of San Andrés frequently visit these islets due to their proximity to the main island. (2) SA has easy access to fishing grounds from the coastline, allowing for shore fishing. This activity is conducted by independent fishers, whose population is not characterized and quantified, and targets multiple species, including parrotfishes, grunts (Haemulidae), and jacks (Carangidae), with unknown catch volumes (Castro, 2005). (3) In 1953, SA was designated as a tax-free region, which promoted an enormous increase in tourism and a significant immigration of people to the island (Meisel, 2003; Abril-Howard et al., 2012a). Artisanal fishery went from local subsistence to a specialized and institutionalized activity based on the local market demand (Olmos, 2019). In contrast, those changes have not significantly impacted PRO (Meisel, 2003; Abril-Howard et al., 2012a). (4) Catch per unit effort (CPUE) in SA has shown a decline since 2009, which has been related to an increase in overfishing on the island (Santos-Martínez, García & Rojas, 2017; Santos-Martínez et al., 2019). Additionally, reports show a greater effort and capture volumes in SA over nearby fishing grounds, including BOL and ALB cays (Castro, Grandas & García, 2007; Rojas et al., 2015). The fishing pressure distinction between BOL and ALB was based merely on their distance from SA.

Results

We recorded a total of 10,438 parrotfishes (6,665 in 2018 and 3,763 in 2019). The most frequently observed species were S. iseri, S. taeniopterus, S. aurofrenatum, and S. viride. As expected, the large-sized species S. coelestinus, S. coeruleus, and S. guacamaia were rare and almost exclusively observed in PRO, the site with the lowest level of fishing pressure. We were able to estimate the total length of 9,788 individuals, corresponding to over 90% of the reported occurrences. Abundance, biomass, and individual body size of parrotfishes varied widely among the islands, species, and sexes (Tables S3 and S4). We present the results per metrics evaluated, emphasizing the general patterns observed per size category under the fishing pressure gradient proposed.

Variation of the individual total length

The best-fitted models for the individual total length had sex, year, species and locality as fixed effects, including the interaction between them and video stations as random effects (Table S2).

From the 2018 data set, the total length of the medium-sized species showed a negative relationship with fishing pressure, with the smallest individuals found on the most heavily fished island (SA, Table S3; Fig. 2A). Sparisoma viride had larger sizes in PRO (β = 4.77, SE = 8.77, p = 1.91e−06; Fig. 2A) and significantly smaller ones in SA (β = −5.39, SE = 9.42, p = 7.25e−08; Fig. 2A). Females of the species reached larger sizes in PRO (β = 5.81, SE = 12.84, p = 0.000275; Fig. 2C), and smaller in SA (β = −4.47, SE = 8.95, p = 8.14e−06; Fig. 2C) while males had greater sizes in BOL (β = 8.45, SE = 3.86, p = 0.00011; Fig. 2B) and smaller in SA (β = −5.98, SE = 11.02, p = 3.11e−09; Fig. 2B). On the other hand, S. vetula had larger sizes in PRO (β = 3.64, SE = 13.01, p = 6.7 e−09; Fig. 2A) and BOL (β = 3.26, SE = 12.34, p = 0.0011; Fig. 2A), with females reaching larger sizes in the former (β = 5.81, SE = 12.84, p = 0.000275; Fig. 2C). In contrast, only the males of the small sized species S. iseri had larger individual body sizes at the most heavily exploited island of SA (β = 3.1, SE = 7.6, p = 0.0019; Fig. 2C). Sparisoma aurofrenatum showed no clear pattern related to fishing pressure, although their individual body sizes presented significant differences among the localities (β = 3.8, SE = 7.34, p = 0.00014).

We found no differences between the 2 years evaluated (DF = 6, F = 1.45, p = 0.19). Nevertheless, in 2019 the differences between localities and species remained the same, with the medium size species showing smaller sizes in SA, including S. vetula (β = −6.01, SE = 8.91, p = 2.13s−09; Fig. 3; Table S4) and S. viride (β = −10.3, SE = 7.53, p = <2e−16), and the small-sized S. iseri having larger sizes in SA (β = 3.73, SE = 6.68, p = 0.0002). In addition, in 2019 we were able to gather a greater sample size of the other two medium-bodied species, and both species showed smaller sizes in SA: S. rubripinne (β = −5.78, SE = 12.01, p = 8.27e−09) and S. chrysopterum (β = −3.49, SE = 10.57, p = 0.00049).

Variation of abundances and biomass

The PERMANOVA applied to parrotfishes abundance in 2018 showed significant differences (DF = 3, MS = 1013.2, F = 1.99, p = 0.01) between SA and the remaining three localities (DF = 30; SA:ALB t = 1.59, p = 0.023; SA:BOL t = 1.52 p = 0.026; SA:PRO t = 1.71, p = 0.026). The results dropped by the SIMPER test showed that the greater abundances of S. taeniopterus females in SA contributed the most to the differences between this island and the other three localities (Fig. 4; Table S5). We also found significant differences in 2019 between SA and PRO in the proportions of the parrotfish composition (DF = 1, MS = 3849.5, F = 4.44, p = 0.002). Likewise, S. taeniopterus females showed to be more abundant in SA and were largely the major contributors to the differences found by the SIMPER analysis (Table S6).

Biomass data showed significant differences (DF = 3, MS = 1903.1, F = 2.81, p = 0.01) between SA and the other three localities (DF = 30; SA:ALB t = 2.28, p = 0.003; SA:BOL t = 1.92 p = 0.012; SA:PRO t = 2.39, p = 0.002). Also, the 2019 biomass data showed SA and PRO to be significantly different (DF = 1, MS = 4045.2, F = 4.57, p = 0.004). In both studied years, the species that contributed most to the overall differences were the small-sized species S. taeniopterus, and the medium-sized species S. vetula and S. viride (Tables S7 and S8). The former had a higher load in the overall parrotfish biomass in SA, while the other two contributed in greater proportion in the other three localities. In addition, at the least exploited site of PRO we found a higher contribution of the medium-bodied species S. rubripinne and S. chrysopterum and the large-bodied species S. coelestinus, S. coeruleus, and S. guacamaia (Figs 5; Tables S6 and S7). As with individual body sizes, no significant differences were found at SA and PRO between the 2 years evaluated in terms of abundances (DF = 1, MS = 929.32, F = 1.57, p = 0.158) and biomass (DF = 1, MS = 851.61, F = 0.9, p = 0.474).

Discussion

Effects of artisanal fishing pressure on parrotfish species populations, sex change, and sex ratios have been previously described (Hawkins & Roberts, 2003, 2004; Hardt, 2009; Vallès & Oxenford, 2014; Vallès, Gill & Oxenford, 2015; O’Farrell et al., 2016). In this study, we have further investigated these relationships under a qualitative fishing pressure gradient, including a comprehensive sample size of eleven species and a high-resolution technique for the underwater assessment of body sizes (diver-operated stereo-video). Overall, our data suggest that fishing pressure is indeed related to the spatial variation in abundance, biomass, and individual body size of the parrotfish species, but most importantly, that there might be indirect effects of fishing pressure on small-sized species.

Following our initial predictions, we expected to find smaller sizes and lower proportions of large and medium-bodied species at a greater fishing pressure. This was indeed the case for most of the species and is consistent with previous studies, where a negative relationship between fishing pressure, body sizes, sex ratios, and abundances were found (Hawkins & Roberts, 2003, 2004; Vallès & Oxenford, 2014; Vallès, Gill & Oxenford, 2015). Likewise, Mixed Effects Models considering sex showed that females of the medium-bodied species S. vetula and S. viride had larger sizes at lower fishing pressure. This finding could be due to selective fishing for large females at the high fishing pressure sites, but it could also indicate that, at least in less exploited locations, sex change occurs at larger sizes than at more heavily fished grounds (Hawkins & Roberts, 2004; O’Farrell et al., 2016). What was most striking, however, were the differences found in the small-sized species S. iseri and S. taeniopterus. We found that parrotfish proportions at the most heavily fished locality showed significant differences with the other three least exploited fishing grounds evaluated and that higher abundances and biomass of S. iseri and S. taeniopterus contributed the most to those differences. Furthermost, this is the first documented study, to our knowledge, to record larger individual sizes of a small-sized parrotfish species at a heavily fished locality, as is the case of the males of S. iseri in SA.

Differences found in biomass are certainly driven by the mentioned changes observed in the abundances and individual body sizes. The higher proportion of small-sized species in the total assemblage of parrotfishes predicted at the beginning of this work is not only a product of a lower contribution of individual body size and proportions of medium and large-bodied species but also an outcome of the higher abundances and individual body sizes of small species. We consider that the higher contribution of S. iseri and S. taeniopterus in the most heavily fished locality suggests an indirect effect of fishing on these two small-sized parrotfish species. Dulvy et al. (2004) suggested that indirect effects of fishing pressure may be due to reduced predation or interspecific competition. In theory, once predators are removed from the ecosystem, their preys should increase as there is no control over them, yet, there is no clear evidence of this relation (Clua & Legendre, 2008). Some studies have found no changes in preys after the demise of predators (Jennings & Polunin, 1997; Taylor et al., 2018; Roff et al., 2019). Other authors have linked greater biomass of predators such as Epinephelus striatus with smaller sizes of S. iseri and S. aurofrenatum (Mumby et al., 2006). In our study, although the greater size and abundance of S. iseri and S. taeniopterus due to lower predation in SA cannot be completely ruled out and requires further examination, to our knowledge, there are no potential predators that may be significantly more abundant in BOL, ALB, and PRO in contrast to SA. Also, as described by Mumby et al. (2006), we should have found greater sizes of the other small-sized species (i.e., S. aurofrenatum, which is smaller than S. taeniopterus) at the locality with supposedly fewer predators due to higher fishing pressure (SA); still, this was not the case.

Instead, we believe that competitive release might be playing a role in the results found with S. iseri and S. taeniopterus. Through stable isotope analysis and intestinal content, Dromard et al. (2015) recognized an overlap in the trophic niche between S. vetula, S. viride, S. iseri and S. taeniopterus. Therefore, it could be argued that when the medium-bodied species (i.e., S. vetula, S. viride) are removed from the system, the small-bodied ones (i.e., S. iseri, S. taeniopterus) may be favored, as some resources for which they actively compete become more available. Consequently, in an intensely exploited locality such as SA, small species can reach larger sizes and higher abundances than in less exploited localities, where larger species limit the resources they compete for. In addition, Hawkins & Roberts (2004) found greater abundances of the smallest species of parrotfish (S. atomarium) in Jamaica, the most heavily exploited island in their study. The intense pressure exerted on parrotfishes in Jamaica has been documented (Hardt, 2009), and we wonder if SA, the most heavily exploited island considered in our study, is showing a step in a chain of changes that follows as parrotfishes are gradually depleted according to sizes of interest for fisheries. Hence, it is essential to monitor parrotfish populations in the Reserve as small size species, like S. aurofrenatum, may become of interest to fisheries. Such monitoring may also give insights into phase shift processes in coral reefs as S. aurofrenatum is a critical consumer of the seaweed Dyctiota in the Caribbean reefs (Dell et al., 2020), a highly opportunistic algae and a great competitor of corals (Fong et al., 2003).

The differences found in parrotfish assemblages can likely influence many biological traits of the species, such as reproduction, but also at the ecosystem level. On the one hand, given the positive relationship between body length and egg production, the reduction of mean body sizes of parrotfish populations due to overfishing is probably negatively affecting their reproductive productivity (Hawkins & Roberts, 2004). On the other hand, the differences found in this study could have a flow-on influence on ecosystem functions (Bonaldo & Bellwood, 2008; Robinson et al., 2019; Shantz, Ladd & Burkepile, 2020). Larger individuals of parrotfishes have greater roles in processes like bioerosion, corallivory, and grazing of certain macroalgae (Bonaldo, Hoey & Bellwood, 2014). Shantz, Ladd & Burkepile (2020) found that the removal of large parrotfish on Caribbean coral reefs increases the abundance of macroalgae and decreases the growth of massive and reef-building corals. This result suggests that it should be necessary to protect fishes larger than 20 cm to maintain their functional diversity. Hence, the functional roles of large parrotfish species are not necessarily replaced by higher abundances or larger sizes of the small-sized species. Bioerosion and coral predation are two ecological functions highly susceptible to overfishing as their rates increases with the body size of parrotfishes (Bellwood, Hoey & Hughes, 2012). Scarus vetula and S. viride are important bioeroders (Bruggemann et al., 1996), and they had smaller sizes in SA; this could cause lower bioerosion rates at the locality. Concerning the consumption of algae, recent studies show that species not consistently considered as part of the herbivore community in the Caribbean, such as Acanthurus coeruleus, Acanthurus tractus, and Kyphosus spp., are critical consumers of macroalgae (Duran et al., 2019; Dell et al., 2020), which are the type of algae that are dominating degrading coral reefs (Perry et al., 2018). Consequently, future studies should include these groups of herbivores to determine the effect of herbivores removal on the ecosystem function.

Our findings did not show significant differences between the 2 years evaluated. However, sampling efforts differ between years as a greater number of shallower stations nearby seagrass meadows were examined in both localities (SA and PRO) in 2019. Therefore, it is relevant to continue monitoring the parrotfish populations, hopefully at the same stations to accurately evaluate possible differences in time. Nonetheless, our sampling effort was balanced between the localities in 2019 and allowed us to gather a greater sampling size of S. rubripinne and S. chrysopterum. Those two medium-sized species had smaller sizes in the most heavily fished locality. At present, neither of these two species has a threat category assigned in Colombia (Chasqui et al., 2017), and it is premature to speak of threat due to fishing pressure when their comparable data is only given in two localities. However, it is important to consider that S. chrysopterum had a negative relationship with fishing pressure (Vallès & Oxenford, 2014) and, according to a report from the continental shores of Colombia, it is one of the most captured species of parrotfishes (INVEMAR-MADS, 2017). Therefore, we recommend increasing the sampling effort by focusing on gathering data of both species on a temporal and spatial level to better understand the differences in our study.

Finally, among the study limitations, different factors were not considered that may influence fish herbivore species’ body size and abundances. Such items may include habitat quality, food availability, and other environmental variables. In some studies, factors such as productivity, temperature, rugosity, latitude, geomorphological attributes of reef formations and slope have shown weak relationships with parrotfish community changes (Cinner et al., 2013; Taylor, 2014; Taylor et al., 2018). In contrast, coral cover and position of coral reefs seem to be related to changes in biomass and abundance of parrotfishes (Hoey & Bellwood, 2008; Nash et al., 2012). Exposed reefs have greater biomass of parrotfishes and erosion levels (Russ, 1984; Gust, Choat & McCormick, 2001; Hoey & Bellwood, 2008; Taylor, 2014; Taylor et al., 2018; Roff et al., 2019). Our findings show that S. vetula and S. viride reach larger sizes in the less fished locality (PRO) and in BOL, with males of S. viride reaching larger sizes in the former. Larger sizes and levels of bioerosion of both species are associated with exposed reefs (Koltes, 1993; Bruggemann et al., 1996; Clements et al., 2017), and BOL seem to have more exposed environments than the other localities (Gamboa et al., 2012) which could explain why such differences were found in this site. Consequently, differences in body size are explained by different factors such as reefs’ exposure, resource availability, and demographic characteristics of fish stocks influenced by external stressors such as fishing exploitation. Future efforts should include environmental factors such as reef exposure and coral cover to account for our study’s intraspecific variation in body size.

Conclusions

Abundances, individual body sizes and biomass of parrotfish species showed significant differences and varied widely depending on the fishing pressure gradient and the size category of the species. On the one hand, medium and large-bodied species of parrotfishes had a negative relation between fishing pressure and contribution to the overall biomass, occurrences, and individual body sizes. On the other hand, we found a significant contribution of the small-size species evaluated to the overall biomass at higher fishing pressure sites. The such greater contribution was driven by the reduction of sizes and abundances of medium and large-bodied species, directly affected by fisheries but was also a product of greater abundances and, most interestingly, larger sizes of the small-sized species. We suggest this result points to indirect effects of overfishing and that such effects could related to a possible case of competitive release. It is relevant to establish how such variations are linked with possible effects on the species’ reproductive productivity and ecosystem processes.

Overall this study provides insights into intraspecific variation in body size, and our substantial volume of data adds to the existing literature on the extent of variation in parrotfish assemblages over relatively short distances. While we consider our general results are better explained under a fishing pressure perspective, this by no means denies the influence of other factors such as inter-island environmental differences. Therefore, although the direct and indirect effects of fishing pressure suggested by our work deserve attention, they should be taken as preliminary until further examination on a temporal and spatial scale is conducted.

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