<<

and predatory relative abundance in three locations of the SeaFlower Biosphere reserve using BRUVS

Miguel Esteban Rodríguez Barragán Estudiante Carrera de Biología Universidad de los Andes

Trabajo de Grado

Director: Diego Cardeñosa Subdirectora: Susana Caballero

Departamento de Ciencias Biológicas

Universidad de Los Andes

14/07/2020

Abstract

Marine are essential to human populations and to ensure their sustainability, it is necessary to understand species interactions in the and how human exploitation are affecting them. Through the , and predatory play important ecological roles as apex and mesopredators but are also an important resource. Estimating the relative abundance of these ecologically and economically valuable species can be used to assess conservation efforts and guide their management. This study aims to estimate and compare the relative abundance of sharks and fishing resources along three areas of the

Seaflower biosphere reserve (Albuquerque, Providence, and Serranilla) where fishing represents an important economical source, using the BRUVS methodology. Data were collected from 2017 to 2019, a total of 141 videos were analyzed and the relative abundance variable was measure by the MaxN index. It was found that there was a relatively low abundance of Lutjanidae (snappers) and (), especially in Serranilla, which should catch the attention of the authorities so can be controlled effectively.

In contrast, Carangidae (Jacks) showed high relative abundance in the three reefs. Relatively high abundance of Caribbean reef shark (Carcharhinus perezi) was found in the three reefs but the highest abundance was found in Providence. There were also few observations of

Tiger shark (Galeocerdo cuvier) & Hammerhead Shark (Sphyrna mokarran). These two big size shark species should be monitored for future studies and to suggest conservation initiatives. In general, it is suggested that more effective controls and regulations should be implemented in the Biosphere reserve as well as a joint work with local fishermen, whose support is the most important asset so that conservation efforts can be successful.

Key words: Sharks, conservation, fisheries, abundance, Seaflower, mesopredators

Introduction

Worldwide, marine ecosystems provide essential services and goods to human populations, but these ecosystems have been negatively affected by human exploitation, making them an important conservation asset in order to ensure their future sustainability

(Worm et al., 2006; Levin & Lubchencho, 2008). To achieve the correct conservation and management of marine resources it is necessary to understand the complex feedback mechanisms and interactions among species within a community or ecosystem (Auster et al.,

2013). Some of the most important interactions that regulate marine ecosystems are trophic chains in which the presence of apex predators and mesopredators can affect and regulate the entire community (Roff et al., 2016)

Among the sea, sharks and predatory fishes play important ecological roles in maintaining normal ecosystems. Sharks are commonly thought to be apex predators, but this classification is sometimes mistaken as not all the species have this role (Roff et al.,

2016). The trophic position of sharks can be classified depending on the body size of the shark; long size shark species e.g. tiger shark (Galeocerdo cuvier), are usually considered apex predators that migrate from coastal to pelagic or to ecosystems (Aines et al.,

2017). These movements generate a large-scale nutrient flux between coastal and oceanic ecosystems (Roff et al 2016). On the other hand, in Caribbean tropical reef ecosystems, predatory fishes such as large (e.g., groupers, snappers, , , jacks) and medium sized sharks such as the Caribbean reef shark (Carcharhinus perezi), act as mesopredators and also can influence the structure of the ecosystem by changing the behavior, species composition and population dynamics of their preys (Estes et al., 2013,

Frisch et al., 2016, Bond et al., 2018). These mesopredators act to control invasive species and provide a small-scale nutrient cycling because of their movements within coral reefs

(McCauley et al., 2012; Roff et al., 2016). Additionally, both apex and mesopredators can reduce the incidence of communal disease in ecosystems by feeding on weak and sick individuals through opportunistic feeding (McCauley et al., 2012). Nevertheless, they also are economically important organisms to both artisanal and industrial fisheries.

Fishing resources have been recognized as an important asset in the accomplishment of the non-hunger and non-malnutrition goal of the Food and Agricultural Organization of the United Nations (FAO) because, from the total global fishing resources extracted, 88% constitute a direct human consumption while 12% belongs to fish derivative product such as fish oil (FAO, 2018;). However, even though the importance of the resource has been recognized, at least 29% of the fish stocks are being fished in an unsustainable way and close to 60% of fish stocks are at full extraction capacity (Matera., 2016). Additionally, it has been found that shark populations are decreasing due to the activities worldwide that are mainly related with Asian shark fin trade. For instance, it is estimated that approximately

100 million sharks are captured every year for fin trade (Worm et al., 2013), including shark species that are listed in CITES (Convention of international Trade in Endangered Species of Wild Fauna and Flora)

To guide the management of ecologically and economically valuable species, it is necessary to generate relevant information such as relative abundance estimates (Ripple et al., 2017, 2015; Palmer et al., 2018). In general terms, abundance refers to the number of individuals of a species that inhabits a given area, which provides information about important changes in ecosystems (Schmeller et al., 2017; Authier et al., 2018) and can be used for assessing conservation efforts, managing wildlife areas, setting fishing or harvesting quotas, among others (Palmer et al., 2018). There are two ways in which abundance can be measured: the absolute abundance and the relative abundance. The absolute abundance is reported more infrequently and presents uncertainty because of the difficulty in detecting all individuals of a species in an area, making it hard for statistical analysis to detect significant changes (Jewell et al., 2012). On the contrary, relative abundance is reported with more frequency increasing the robustness of statistical analyses when utilized (Authier et al.,

2018). Indeed, in Colombia, there is a lack of specific fishing statistical information of large groups of fishes such as groupers, snappers, or sharks, which complicates the study of fishing impact on fish populations (Chasqui et al., 2017). Additionally, the infrequent and poor fishing data collection, makes fisheries management a challenging topic to the point that risk extinction estimates of Colombian marine fishes are mainly based on expert’s knowledge of species and fisheries, and some indicators which are not always precise (Chasqui et al., 2017).

In the case of assessing marine wildlife relative abundance, Baited Remote

Underwater Videos (BRUV) have gained popularity because they are relatively cheap, non- extractive, non-invasive and non-destructive. This methodology is useful for accessing a wide range of depths and habitats, recording rare and elusive species (L de Vos et al., 2015) and observe other features such as behaviors, amount of , species richness

(Whitmarsh et al, 2018) (Harvey et al 2013).

The Seaflower Biosphere Reserve (SBR) is a set of islands located in the north of the

Colombian territory. It was declared a biosphere reserve in the year 2000 by UNESCO and has an approximate area of 180000 km2 (Coralina, 2016). This reserve hosts many different ecosystems, including the world´s third largest coral barrier reef (Garay et al., 1987; Alvarez et al., 2019). In 2005, the Colombian national government declare Seaflower as a marine protected area (MPA), which is a delimitated geographical area dedicated to the protection, conservation, and restoration of a marine ecosystem and its resources (Guarderas et al., 2008; CCO, 2015; Sanchez et al., 2019). The MPA is divided into three sectors, north, central, and south. The north sector has an area of 37000 km2 and constitutes of Serrana, Roncador, and

Quitasueño; the central sector has two islands: Providencia and Santa Catalina with an area of 12700 km2; and finally, the south sector consists of San Andres, Bolivar Cay, and

Albuquerque cay and has an area of approximately 14800km2 (Coralina, 2016; Sánchez-

Jabba, 2012).

In Seaflower there are many income generating activities such as tourism, commerce, wage labor, property rental, agriculture and fishing (Matera, 2016). In the reserve, there are

273 species of reef-associated fish that have been identified including species from the

Carangidae family and the Lutjanidae family which are economically important to both artisanal and industrial fisheries. Observed also are species that have been listed in the IUCN red list such as hogfish (Lachnolaimus maximus); mutton snapper (Lutjanus analis); among others. Due to unsustainable fishing, the majority of the big sized fishes (>1m) have been extracted which has resulted in the gradual shift to targeting smaller fishes whose size is in the range of 30 to 40 cm, since they become the next best economic income. Unfortunately, such practices interrupt their reproductive cycles causing downstream effects on the viability of a population (Jacobsen et al., 2014; Polanco & Acero, 2019).

Artisanal fishing satisfies the local market demand, representing an important source of food for local households and providing local fishermen part of a basic income to sustain their needs (Matera, 2016). On the other hand, commercial fishing is practiced in order to satisfy an international demand, which means a larger capacity to extract resources and a stronger impact on the ecosystem (Sánchez-Jabba, 2012). The latter fishing method can only be practiced in the northern part of the SBR (Aguilera, 2010; Sánchez-Jabba, 2012).

Considering that an MPA principal objective is to allow the sustainable exploitation of resources while preserving the ecosystems, it is necessary to generate relevant information about fish stocks. For example, as shown by Speed, Cappo & Meekan (2018) and Garla et al. (2006), MPA have been successful to help in the recovery of sharks and predatory fish populations. Generating this information in the biosphere reserve will provide a baseline for assessing conservation efforts and management of shark populations and local fisheries.

Hence, this study aims to estimate and compare the relative abundance of sharks and fishing resources along three areas of the Seaflower biosphere reserve (Albuquerque, Providence, and Serranilla) using the BRUVS methodology.

Materials and Methods

Study site and Background

Seaflower is a biosphere located at the Colombian Caribbean Sea, it hosts a great variety of ecosystems such as tropical dry forest, mangroves, and seagrasses.

Seaflower host approximately 77% of the shallow Colombian coral reefs (Invemar, 2002;

Coralina 2015). Most importantly, the worlds third-largest coral reef is in this area, which hosts a great variety of marine species. It is conformed by three inhabited main islands: San

Andrés, Providencia, Santa Catalina, 6 minor islands/cays at north: Quitasueño, Serrana.

Serranilla, Roncador, Bajo Nuevo y Bajo Azul, and 2 islands at south: Albuquerque and

Bolivar (CCO 2015) as can be seen in Figure 1.

Seaflower is known to possess a high biodiversity index in the Caribbean, thereby it constitutes an important area with a great environmental value. Economically, this area has an important value because of the industrial and artisanal activities that due to poor regulation, have caused a decrease in fishing resources. In previous expeditions (Seaflower expedition, 2014) different dives showed that the most abundant shark in the area is the nurse shark (Ginglimostoma cirratum) and the gray shark (Carcharinus sp) (CCO, 2015).

In this study, BRUVS were deployed along three islands: Providence, Serranilla, and

Albuquerque to determine the relative abundance of sharks and predatory fishes. This study represents an important step in determining shark and predatory fish abundance in the

Biosphere reserve since it might be an important ecological area.

Figure 1. Seaflower Biosphere Reserve map big red circle and the three study sites: Serranilla black circle green pin; Providence red square red pin; Albuquerque blue triangle yellow pin. The black dot line represents a non MPA

Data collection

Baited remote underwater videos BRUVS, consists of a galvanized or aluminum frame with an internal GoPro camera that is placed and programmed to record for 90 minutes.

A 1.5 m long pole that holds the bait is attached to the galvanized/aluminum frame. In this study the bait contained 1kg of crushed according to the methodology presented in the study of Whitmarsh (2018), Harvey et al. (2013), Winter & De Graff (2019). BRUVs were deployed between 2017 and 2019 at different random points around Providencia, Serranilla, and Albuquerque. Additionally, the BRUVs system was deployed at different depths and >400 m apart in order to avoid overlapping (Speed, Cappo, Meekan 2018).

Data analysis

The obtained videos were reviewed using VLC media player (V3.0.11) Time started to run when the BRUV landed on the seafloor, where it remained still and it was left until it completed the target deployment time (90 min). In order to avoid pseudoreplication measuring relative abundance, the maximum number of individuals of same species appearing at the same time was taken as the abundance data measure, which has been used in previous studies (Jabado et al 2018) and is known as MaxN which is an estimate of abundance used in high-density population sites such as coral reefs (Cappo et al 2003). The species recorded were identified to the lowest possible taxonomic level using an online fish guide for Caribbean fish species (reefguide.org). In this study, herbivore fish species were not considered, on the contrary we observed predatory fish groups such as groupers, snappers, jacks, mackerels and sharks. In cases where species identification was not completely ensured, the individuals were identified to the closest genus or family name.

For the statistical analysis, the program R (V 4.0.1) was used in order to perform a

Kruskall-Wallis non-parametric test to determine if a fish group MaxN was significantly different between reefs and when results were significant, a post-hoc Dunn test was performed to look at among reef differences in MaxN and the respective p-values.

Figure 2. BRUVS visualization. Sphyrna mokarran (left) and 3 Carcharhinus perezi (right)

Results

A total of 141 videos (Albuquerque 41, Serranilla 47, and Providence 52) were analyzed. For snappers, four species were identified: yellowtail snapper (Ocyurus chrysurus), schoolmaster snapper (Lutjanus apodus), dog snapper (Lutjanus jocu) and mutton snapper

(Lutjanus analis). Also, six species of groupers were identified in this study: coney

(Cephalopholis fulva), black grouper (Mycteroperca bonaci), redhind grouper (Epinephelus guttatus), grasby grouper (Cephalopholis cruentata), yellowfin grouper (Mycteroperca venenosa), and yellowmouth grouper (Mycteroperca interstitialis). For jacks, only three species were recorded: bar jack (Carangoides ruber), yellow jack (Carangoides bartholomaei), and horse-eye jack (Caranx latus). Finally, only one species of and could be observed: (Sphyraena barracuda) and cero mackerel

(Scomberomorus regalis), respectively.

We divided fish categories into eight groups: C. perezi, Snappers, Snappers no- yellowtail, Small grouper, Large grouper, Jacks, Barracuda and Mackerel. (see Table 1). The small grouper fish group included species such as Coney, Grasby, redhind, and the large grouper fish group included species such as yellow, tiger, and the Mycteroperca genus. For the snapper group, the individuals were divided into snappers and snappers no yellowtail

because the latter are more common and do not have an important economic value. From

the 141 deployments, sharks and rays were observed in 136 videos which represent 93% of

all videos recorded. A total of six shark species (C. perezi, G. cirratum, Rhizoprionodon sp

G. cuvier, S. mokarran, C. acronatus,). Caribbean reef shark (C. perezi) was the shark species

that showed the greatest relative abundance in all three reefs even more than G. cirratum,

which is a shark species known for its wide distribution (Garla et al 2016) (Pratt et al 2018).

C. perezi was observed in 103 of the 145 videos (porcentaje del total %) and G. cirratum in

73 of the 145 total videos (porcentaje del total %). The total shark sightings can be observed

in Table 2.

Table 1. Total fish sightings per fish group found in the BRUVS deployments in Serranilla, Albquerque and Providence in the Seaflower Biosphere Reserve

Fish Group

Snappers no Small Large Reef C. perezi Snappers yellowtail groupers groupers Jacks Barracudas Mackerels Serranilla 44 64 6 61 0 189 21 1 Albuquerque 58 131 53 114 9 120 35 6 Providence 71 122 58 61 33 191 28 8

Table 2. Total shark sightings per shark species. C. perezi found in the videos in the islands of Providence, Serranilla and Albuquerque in the Seaflower Biosphere Reserve Shark species Rhizoprionodon Total Reef C. perezi G. cirratum sp. G. cuvier S. mokarran C. acronotus Serranilla 44 39 46 1 2 1 133 Albuquerque 58 28 17 0 2 0 105 Providencia 71 31 2 1 2 0 107 Total 173 98 65 2 6 1 345

For the statistical analysis, only C.perezi was compared with the other fish groups

since the others shark species did not represent a significant number of sightings in MaxN

and in the specific case of G. cirratum, it is a well studied species and its relative abundance was not unexpected since it is well reported that this species is widely distributed in the

Caribbean. The Kruskal-Wallis test showed that there were significant differences between the different fish groups studied and the three reefs (see Table 3) with the exception of

Mackerels, which did not present a significant p- value (0.0819>0.05). A Bonferroni correction was used for the Dunn test that resulted in significant differences between reef- reef comparisons and fish groups (see Table 3). The significant values of the statistical test for each comparison between the study areas and fish groups can be observed in (see Table

3). Serranilla showed the lowest relative abundance and Average of MaxN for most fish groups observed, compared to providence and Albuquerque, which results in Serranilla having more significant differences with the other two sites. The comparison of the MaxN index for each fish group (represented as the average of MaxN), and the study sites is shown in figure 3.

Table 3. Reef-reef significant differences. Kruskall-Wallis test and Dunn test with the Bonferroni correction

K Wallis Test Dunn Test

Comparison

Fish group Chi Squ p-value z Pr(>|z|) Providence - Albuquerque 2,285 0,066851 Barracuda Serranilla - Albuquerque 9,09 0,0106 2,897 0,011312 Serranilla - Providencia 0,704 1 Providence - Albuquerque 1,378 0,5050722 Snapper Serranilla - Albuquerque 12,099 0,00236 3,428 0,0018269 Serranilla - Providencia 2,21 0,0813426 Providence - Albuquerque 0,398 1 Snapper noyellowtail Serranilla - Albuquerque 46,636 7,47E-11 5,927 9,25E-09 Serranilla - Providencia 5,88 1,23E-08 Providence - Albuquerque 4,91 2,74E-06 Small Grouper Serranilla - Albuquerque 27,931 8,61E-07 4,321 4,66E-05 Serranilla - Providencia 0,507 1 Providence - Albuquerque 2,838 0,013629 Large Grouper Serranilla - Albuquerque 25,407 3,04E-06 1,938 0,157863 Serranilla - Providencia 5,003 1,70E-06 Providence - Albuquerque 2,797 0,015466 Jacks Serranilla - Albuquerque 11,148 0,003795 0,002 1 Serranilla - Providencia 2,901 0,011162 Providence - Albuquerque 0,837 1 Mackerel Serranilla - Albuquerque 5,0046 0,0819 1,28 0,601607 Serranilla - Providencia 2,228 0,077701 Providence - Albuquerque 0,62 1 C.perezi Serranilla - Albuquerque 9,7043 0,007811 2,218 0,0796711 Serranilla - Providencia 2,998 0,0081459

Figure 3. Average of Sum MaxN of every fish group studied (y axis) compared with the 3 reefs studied (x axis). Serranilla is the reef that present the lowest MaxN for large groupers, Barracudas, Mackerels, Snapper noyellowtail, and Snappers.

Discussion & Conclusions

Seaflower Biosphere Reserve SBR represents an important place for local inhabitants that depend on fishing resources as it is their main economic income and their main food source. On the other hand, little is known about the ecological value of the reserve and the species that inhabits this area in the Colombian Caribbean. In this study relative abundance of sharks and predatory fishes were estimated and compared between three islands of the SBR: Serranilla, Albuquerque and Providence, using a non-extractive, non-invasive and easy to manipulate technique known as Baited remote underwater videos (BRUVS). Serranilla showed the lowest relative abundance of fishes that represent an important economical value such as large groupers and snappers noyellowtail. Albuquerque and Providence have similar trends of relative abundance although in Albuquerque there was a relative low abundance of large groupers. The most abundant shark was the Carcharhinus perezi, being more abundant than the nurse shark Gynglimostoma cirratum, a species known for its cosmopolitan distribution and high abundance index worldwide. For sharks, it must be highlighted the observation of two top predators and migrating sharks (Galeocerdo cuvier & Sphyrna mokarran).

The relative low abundance of snappers could be related with the fact that along the three reefs macroalgal coverage was dominant over corals, which is related with coral reef degradation (Hoey et al., 2011; McCook et al., 2001). Although snappers might not directly influence the coral reef they work as an indicator of coral reef degradation (Gamboa et al.,

2019). While some snappers species represent an important asset for many industrial fisheries in the Atlantic Ocean, and, it is common to see them in Florida landings and Brasil (South

Atlantic) fisheries, some species such as the mutton snapper are more common in recreational fisheries and small-scale fisheries (Hope 2015) (Stevens 2018) (Previero & Gasalla 2018).

This makes controls and regulations harder as small-scale fisheries have poor data availability and do not implement continuous or systematic monitoring (Ramirez et al.,

2017). There are many conservation initiatives that could be suggested in order to promote the conservation of snapper fisheries, for example, ethnozoology which has been used in

Brazil and could be applied in this MPA (Messias et al., 2019). In Colombia, snapper species such as Lutjanus synagris are in the red list of threaten species in Colombia this due to the unsustainable fishing in the Colombian Caribbean (Parques Nacionales Naturales de

Colombia, 2015). Also, snappers in 2015 represented the most important fishing resource in

Colombia and its price make of it an objective fishing resource (Gutierrez, 2010; Amado et al., 2015). Also, as the snapper market become important in the last years, it was suggested that efforts should be focus in farming snappers (Gutierrez. 2010; Amado et al.,

2015), however it has conservation implications as farmers take juveniles from the wild which could end in a decline of snapper populations in the wild.

Groupers represent a valuable market product but overfishing by both industrial and artisanal fisheries as well as habitat degradation and pollution have caused a decline in groupers population. This results in fisheries targeting new taxa such as smaller species and juveniles of larger species, sometimes taken as bycatch and in other cases to reproduce them in the aquaculture business (De Mitcheson et al., 2020). Also, features like being long lived, having late sexual maturation and aggregation spawning of the life history of groupers makes them susceptible to overfishing pressures, (De Mitcheson et al 2013). This is a topic of great concern since it has been observed that fish species are getting smaller due to the selective pressures imposed by modern overfishing techniques (Conover et al 2009). However, the changes induced by human exploitation can be reversed by implementing policies and controls such as regulating the minimum catch size allowed, a fishing quota, and specific fishing seasons for small- and large-scale fisheries (Beddington & Retting,1983; Anderson,

2019). Besides, in some cases this fish is worth more alive than as a food, which is the case of the Epinephelus striatus and Epinephelus itajara (VU by IUCN), species that represent a great value both because for many commercial dive operations (Shideler & Pierce 2016).

The relative high abundance of jacks could be associated with their migratory season, and that this migration is done in groups. Also, it represents an important economic source for artisanal fisheries which have a low impact on fish populations compared with industrial fisheries (Caiafa et al., 2011; Alfaro et al., 2016). However, as stated before, small scale fisheries represent a challenge in terms of regulation and control. During the last years, this fish group gain important value in the local market (Alfaro et al., 2016) therefore it is important to keep studying this fish populations as well as their biological cycle so conservations efforts can be focused in the right direction taking into account the preferred size of consumption, their reproductive cycle and their life history. Also, since they are migratory species along the Caribbean, the use of acoustic telemetry could be a useful tool to track this fish populations. This is a relatively new technique that has been used for fisheries management in different regions in the Caribbean (Crossin et al., 2017)

It is important to highlight that the relatively high abundance of the C. perezi. observations included both males and females, adults and juveniles. This shark species spends a large part of its life cycle in coral reefs and is rarely seen out of them (Bond et al.,

2012). However, it has been suggested that more studies are necessary to understand the complex habitat use that this shark has developed, in order to focus the conservation planning in the correct way (Brooks et al., 2013). For conservation purposes, future implementation of a reserve could be an effective approach to protect this shark species since it has been observed that reserves are vital in reef shark conservation (Bond et al., 2012; Dwyer et al.,

2020). Although Seaflower is a reserve there are currently not enough controls to effectively enforce policies. Another way to protect this shark is by sustainable ecotourism (Dive sightings). Study of the C.perezi population in this area of the Caribbean is important to understanding and learning the ecological role of this shark. However, Bond et al (2018) concluded that in the Colombian Caribbean, this shark is a mesopredatory species and plays a similar ecological role to that of predatory fishes. Considering that there is a decline in predatory fish populations, it could be suggested that C. perezi could replace the role of predatory fishes and occupy their niche.

For the other large shark species observed, although with fewer observations (G. cuvier n = 6 & S. mokarran n= 2). It is important to keep monitoring the area to see if there are more observations of these species in the next years which could highlight the importance of the Biosphere Reserve for attracting ecologically important apex predators. Tracking and tagging these migratory sharks could open a path to new conservation strategies that aim to protect the migratory routes as they are important in shark life cycles (Dunn et al., 2019).

Providence

From the studied places, it was expected that Providence would show the lowest relative abundance of every fish group since it is the second most populated island in the

Biosphere reserve after San Andres. In 2016, up to 1200 locals depended on marine resources as their main source of income and protein. Also, it is estimated that close to 90% of the households depend mainly on marine resources as their primary source of income (Matera,

2016). The effect of human activities on marine resources has previously been studied, showing a negative correlation between fish populations and human activities which has resulted in up to 40% reduction of the fish biomass (Valdivia et al 2017). However,

Providence locals are concerned about conservation topics and understand the importance of marine resources at the point that the great majority of them support the establishment of the

MPA, although, there are some that know little about what an MPA is and how it regulates fisheries. fisheries in Providence are categorized as artisanal fisheries, this means that the fishermen extract marine resources only for their income and main food source (Matera

2016). This could explain the relative higher abundance of some fish groups when compared to areas with industrial scale commercial fishing. In contrast, small groupers showed a low relative abundance in this area, which possibly means that fishermen are fishing these individuals at a higher rate, but this needs to be confirmed by further studies. The fishery management efforts in providence are strong and the local government continues to monitor the fishermen activities.

Albuquerque

Albuquerque showed similar trends in fish relative abundance as Providence.

However, large groupers presented a low relative abundance index in comparison to

Providence. This might be due to overfishing pressure since the area that surrounds

Albuquerque is relatively close to central American countries that depend on fishing resources (Salas et al., 2011). Additionally, although there is not a strong tourism pressure in the area, it is an invasive practice that can result in the damage of coral reefs that host a great biodiversity of marine species including groupers. According to De Mitcheson et al. (2020) groupers are currently going through a high fishing pressure due to their economic value and this highlights the need of strong regulation in order to allow the population’s recovery.

Serranilla

The lack of control and regulation is evident in the Serranilla reef, where more significant differences in relative abundance index were found compared with the other reefs.

Geographically, Serranilla is the furthest island in the biosphere reserve and there is no knowledge of an established local population which suggests that unregulated fishing activities are the primary source of ecological degradation. These fisheries could be both artisanal and industrial and could be performed by local or foreign fishermen (Puentes et al.,

2014) that take advantage of the lack of MPA policies and regulation extracting marine resources in an unsustainable way. According to the results obtained here, the most affected fishes are large and small groupers and snappers, which may be because these are economically important species in many markets (Salas et al., 2011) as has been observed in the reports of the Caribbean landings (Begossi et al., 2012; Simock, 2017). This territory has not been studied completely and fish populations trends around the area have not been examined yet, leaving a gap in where overfishing could lead to an important decline of fish resources. It is important then to track the fisheries activities occurring in the area and the establishment of strong controls in which fisheries declare their landings. Nonetheless, the low relative abundance detected can be attributed to the fact that this study area is located in the northern part of the Seaflower Biosphere reserve, which is the only area where industrial fishing is allowed to be performed. This could imply that industrial fishing is having a strong negative impact in the local fish stocks and is affecting the resilience of the MPA.

In Colombia, the national authority of aquaculture and fishing AUNAP is the entity that has control of Colombian fisheries, both artisanal and industrial. However, they do not have fishing data for any of the 3 reefs observed in this study which highlight the importance of estimating fish size populations and trends especially if there are places where fish landings have been reported previously by the AUNAP in San Andres and Providence.

Additionally, for Scombridae (Mackerels) and Sphyranidae (Barracudas) families there are few studies and reports related to the fishing activities of these three groups. In the AUNAP website there are not reports related to any these group of fish in the study area, so it is difficult to determine the real population status and trends. However, monitoring this fish groups is important because as fish stocks decline worldwide, these groups might become in the next target fishing resources (Jul-Arsen, 2003; Teh et al., 2017).

The study area represents a huge MPA which by IUCN definition is a “clearly defined geographical space, recognized, dedicated and managed, through legal or other effective means, to achieve the long-term conservation of nature with associated ecosystem services and cultural values” (IUCN, 2008). Understanding fishing resource populations is a vital topic for conservation efforts, as it is necessary to determine the health of the marine ecosystems, so the correct conservation efforts and policies can be implemented while maintaining a mutual benefit of the protected area and the locals inhabiting it. The Biosphere

Reserve Seaflower constitutes a multiple-use MPA, which means that while being a protected area, it should also be able to provide the local human population and support their social and economic needs (Matera, 2016). Here we observed predatory fishes that have important ecological and economical roles making it imperative to develop a sustainable fisheries resources usage in order to ensure the preservation of the ecosystems occupied by these species (Emslie, 2017). This can be achieved by working with local fishermen and explaining sustainable fishing methods, appropriate time of the year to extract each fish species and the preferable size (adult) in which a fish must be consumed.

Finally, there is a need to implement stronger regulations and policies along the

Biosphere Reserve, so it is guaranteed that fishing is being carried out responsibly and sustainably. This, combined with educational campaigns in which locals and scientist share their knowledge may lead to effective conservation efforts which will benefit both, the locals and the marine ecosystem. Perhaps the most important goal must be that the local community supports the conservation campaigns, because without their support all conservation efforts might be useless.

References

Aines, Alexandra & Carlson, John & Boustany, Andre & Mathers, Alyssa & Kohler, Nancy. (2017). Feeding habits of the tiger shark, Galeocerdo cuvier, in the northwest Atlantic Ocean and Gulf of Mexico. Environmental Biology of Fishes. 10.1007/s10641-017-0706-y

Alvarez-Yela, A. C., Mosquera-Rendón, J., Noreña, A., Cristancho Ardila, M. A., & López- Alvarez, D. C. (2019). Microbial diversity exploration of marine hosts at Serrana Bank, a coral atoll of the Seaflower Biosphere Reserve. Frontiers in Marine Science, 6, 338.

Alfaro-Martínez, S., Bustos-Montes, D., Salas-Castro, S., Gómez-León, J., & Rueda, M. (2016). Fecundidad del jurel aleta amarilla, Caranx hippos (Linnaeus) en el Caribe colombiano. Boletín de Investigaciones Marinas y Costeras-INVEMAR, 45(1), 123-134

Amado, A. C.,Ccordoba-Rojas, D. F., & Barbosa, L. S. (2015). Avances de acuicultura y pesca en colombia volúmen i. retreived from: https://www.researchgate.net/profile/Armando_Ortega_Lara/publication/303193819_Avan ces_de_Acuicultura_y_Pesca_Vol_I/links/5818aab908aee7cdc685bc56/Avances-de- Acuicultura-y-Pesca-Vol-I.pdf

Anderson, L. G. (Ed.). (2019). Fisheries Economics, Volume I: Collected Essays. Routledge.

Auster, P. J., Estes, J. A., & Coleman, F. C. (2013). Species interactions in marine communities: the invisible fabric of nature. Bulletin of Marine Science, 89(1), 3-9.

Authier, M., Dorémus, G., Van Canneyt, O., Boubert, J. J., Gautier, G., Doray, M., ... & Spitz, J. (2018). Exploring change in the relative abundance of marine megafauna in the Bay of Biscay, 2004–2016. Progress in oceanography, 166, 159-167.

Beddington, J. R., & Rettig, R. B. (1983). Approaches to the regulation of fishing effort (No. 240-248). Chapter 3:Techniques for regulating fishing mortality Food & Agriculture Org.

Beer, A. J. E. (2015). Diversity and abundance of sharks in no-take and fished sites in the marine protected area network of Raja Ampat, West Papua, Indonesia, using baited remote underwater video (BRUVs). Royal Roads University (Canada).

Begossi, A., Lopes, P., & Silvano, R. A. M. (2012). Co-management of reef fisheries of the snapper-grouper complex in a human ecological context in Brazil. Global progress in ecosystem-based fisheries management, 1-22.

Bond ME, Babcock EA, Pikitch EK, Abercrombie DL, Lamb NF, et al. (2012) Reef Sharks Exhibit Site-Fidelity and Higher Relative Abundance in Marine Reserves on the Mesoamerican Barrier Reef. PLoS ONE 7(3): e32983. doi:10.1371/journal.pone.0032983

Bond, M. E., Valentin-Albanese, J., Babcock, E. A., Hussey, N. E., Heithaus, M. R., & Chapman, D. D. (2018). The trophic ecology of Caribbean reef sharks (Carcharhinus perezi) relative to other large teleost predators on an isolated coral atoll. Marine Biology, 165(4), 67.

Brooks, Edward & Sloman, KA & Sims, David & Danylchuk, Andy. (2011). Validating the use of baited remote underwater video surveys for assessing the diversity, distribution and abundance of sharks in the Bahamas. Endangered Species Research. 13. 231-243. 10.3354/esr00331.

Brooks, E. J., Sims, D. W., Danylchuk, A. J., & Sloman, K. A. (2013). Seasonal abundance, philopatry and demographic structure of Caribbean reef shark (Carcharhinus perezi) assemblages in the north-east Exuma Sound, The Bahamas. Marine biology, 160(10), 2535- 2546.

Caiafa, I., Narváez, J., & Borrero, S. (2011). Algunos aspectos de la dinámica poblacional del jurel Caranx hippos (Pisces: Carangidae) en Bocas de Ceniza, Caribe colombiano. Revista MVZ Córdoba.

Cappo, M., Harvey, E., Malcolm, H. & Speare, P. Potential of video techniques to monitor diversity, abundance and size of fish in studies of marine protected areas in Aquatic Protected Areas: What Works Best and How Do We Know? (eds Beumer, J. P., Grant, A. & Smith, D. C.) 455–464 (Australian Society of Fish Biology, 2003).

Chasqui, V., Polanco, L. A., Acero, F. A., Mejía-Falla, P. A., Navia, A., Zapata, L. A., & Caldas, J. P. (2017). Libro rojo de peces marinos de Colombia. Instituto de Investigaciones Marinas y Costeras Invemar, Ministerio de Ambiente y Desarrollo Sostenible. Serie de Publicaciones Generales de INVEMAR, 93.

Comisión Colombiana del Océano 2015 CCO Seaflower Reserva de Biosfera Seaflower retrieved from: http://www.cco.gov.co/101-areas/asuntos-marinos/103-seaflower.html

Coralina (2016) Archipiélago de San Andrés, Providencia y Santa Catalina: una reserva de Biosfera en el Caribe Colombiano. Reserva de Biósfera Seaflower: Corporación para el Desarrollo Sostenible del Archipiélago de San Andrés, Providencia y Santa Catalina (CORALINA). San Andrés, Colombia.: Retrieved from http://www.coralina.gov.co/nuevositio/en/areas-protegidas-m

Conover, D. O., Munch, S. B., & Arnott, S. A. (2009). Reversal of evolutionary downsizing caused by selective harvest of large fish. Proceedings of the Royal Society B: Biological Sciences, 276(1664), 2015-2020.

Crossin, G. T., Heupel, M. R., Holbrook, C. M., Hussey, N. E., Lowerre‐Barbieri, S. K., Nguyen, V. M., ... & Cooke, S. J. (2017). Acoustic telemetry and fisheries management. Ecological Applications, 27(4), 1031-1049.

Danell, K., Bergström, R., Duncan, P., & Pastor, J. (Eds.). (2006). Large herbivore ecology, ecosystem dynamics and conservation (Vol. 11). Cambridge University Press.

De Mitcheson, Y., Craig, M. T., Bertoncini, A. A., Carpenter, K. E., Cheung, W. W., Choat, J. H., ... & Liu, M. (2013). Fishing groupers towards extinction: a global assessment of threats and extinction risks in a billion dollar fishery. Fish and fisheries, 14(2), 119-136.

De Mitcheson, Y. J. S., Linardich, C., Barreiros, J. P., Ralph, G. M., Aguilar-Perera, A., Afonso, P., & Nair, R. J. (2020). Valuable but vulnerable: Over-fishing and under- management continue to threaten groupers so what now?. Marine Policy, 116, 103909.

Dunn, D. C., Harrison, A. L., Curtice, C., DeLand, S., Donnelly, B., Fujioka, E., ... & Åkesson, S. (2019). The importance of migratory connectivity for global ocean policy. Proceedings of the Royal Society B, 286(1911), 20191472.

Emslie, M. J., Cheal, A. J., & Logan, M. (2017). The distribution and abundance of reef- associated predatory fishes on the Great Barrier Reef. Coral Reefs, 36(3), 829-846.

FAO. 2018. The State of World Fisheries and Aquaculture 2018 - Meeting the sustainable development goals. Rome. Licence: CC BY-NC-SA 3.0 IGO.

Frisch, A. J., Ireland, M., Rizzari, J. R., Lönnstedt, O. M., Magnenat, K. A., Mirbach, C. E., & Hobbs, J. P. A. (2016). Reassessing the trophic role of reef sharks as apex predators on coral reefs. Coral Reefs, 35(2), 459-472.

Fisheries, F. A. O. (1822). Aquaculture-Cultured Aquatic Species Information Programme. Clarias gariepinus

González-Gamboa, I., Santos-Martínez, A., & Herrera-Martínez, Y. (2019). Potential response of coral reef'S functional structure and snapper abundance to environmental degradation in san andres island, colombia. Acta Biológica Colombiana, 24(1), 86-96.

Garla RC, Chapman DD, Wetherbee BM, Shivji MS (2006a) Movement patterns of young Caribbean reef sharks, Carcharhinus perezi, at Fernando de Noronha Archipelago, Brazil: the potential of marine protected areas for conservation of a nursery ground. Marine Biology 149: 189–199. DOI 10.1007/s00227-005-0201-4.

Jesús, g., francisco, c., carlos, a., jairo, a., luisa, n., de la pava, m. A. R. T. A., ... & germán, m. (1987). Estudio oceanográfico del área insular y oceánica del caribe colombiano archipielago de san andrés y providencia y cayos vecinos. Boletín científico cioh no, 9, 1-33.

Guarderas, A. P., Hacker, S. D., and Lubchenco, J. (2008). Current status of marine protected areas in latin america and the caribbean. Conserv. Biol. 22, 1630–1640. doi: 10.1111/j.1523- 1739.2008.01023.x

Gutiérrez F. P. 2010. Los recursos hidrobiológicos y pesqueros continentales en Colombia. Instituto de Investigación de Recursos Biológicos Alexander von Humboldt. Bogotá. 118 pp.

Garla, R. C., Gadig, O. B. F., & Garrone-Neto, D. (2016). Movement and activity patterns of the nurse shark, Ginglymostoma cirratum, in an oceanic Marine Protected Area of the South- western Atlantic. Journal of the Marine Biological Association of the United Kingdom, 97(08), 1565–1572.

Halpern, B. S., Walbridge, S., Selkoe, K. A., Kappel, C. V., Micheli, F., D'Agrosa, C., & Fujita, R. (2008). A global map of human impact on marine ecosystems. science, 319(5865), 948-952.

Harvey ES, McLeanD, Frusher S, Haywood MDE, Newman SJ, Williams A (2013) The Use of BRUVs as a tool for assessing marine fisheries and ecosystems: a review of the hurdles and potential the university of Western Australia

Heupel, M., Knip, D., Simpfendorfer, C., & Dulvy, N. (2014). Sizing up the ecological role of sharks as predators. Marine Ecology Progress Series, 495, 291–298. doi:10.3354/meps10597

Hoey, A. S., Pratchett, M. S., & Cvitanovic, C. (2011). High macroalgal cover and low coral recruitment undermines the potential resilience of the world's southernmost coral reef assemblages. PLoS One, 6(10), e25824.

Hope, J; Muller, R & Addis, D. 2015 SEDAR update Assessment, Stock Assessment of Mutton Snapper (Lutjanus analis) of the US South Atlantic and Gulf of Mexico through 2013.

Jabado, R. W., Al Hameli, S. M., Grandcourt, E. M., & Al Dhaheri, S. S. (2018). Low abundance of sharks and rays in baited remote underwater video surveys in the Arabian Gulf. Scientific Reports, 8(1). doi:10.1038/s41598-018-33611-8

Jacobsen, N. S., Gislason, H., & Andersen, K. H. (2014). The consequences of balanced harvesting of fish communities. Proceedings of the Royal Society B: Biological Sciences, 281(1775), 20132701.

Jewell, R., Thomas, L., Harris, C. M., Kaschner, K., Wiff, R., Hammond, P. S., & Quick, N. J. (2012). Global analysis of cetacean line-transect surveys: detecting trends in cetacean density. Marine Ecology Progress Series, 453, 227-240

Jul-Larsen, E. (Ed.). (2003). Management, Co-management, Or No Management?: Major Dilemmas in Southern African Freshwater Fisheries (Vol. 422). Food & Agriculture Org.

L De Vos, RGA Watson, A Götz & CG Attwood (2015) Baited remote underwater video system (BRUVs) survey of chondrichthyan diversity in False Bay, South Africa, African Journal of Marine Science, 37:2, 209-218, DOI: 10.2989/1814232X.2015.1036119

Levin, S. A., & Lubchenco, J. (2008). Resilience, robustness, and marine ecosystem-based management. Bioscience, 58(1), 27-32.

Matera, J. (2016). Livelihood diversification and institutional (dis-)trust: Artisanal fishing communities under resource management programs in Providencia and Santa Catalina, Colombia. Marine Policy, 67, 22–29.

McCook, L., Jompa, J., & Diaz-Pulido, G. (2001). Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral reefs, 19(4), 400-417.

Messias, M. A., Alves, T. I., Melo, C. M., Lima, M., Rivera-Rebella, C., Rodrigues, D. F., & Madi, R. R. (2019). Ethnoecology of Lutjanidae (snappers) in communities of artisanal fisheries in northeast Brazil. Ocean & Coastal Management, 181, 104866.

Mourier, Johann & Planes, Serge & Buray, N. (2012). Trophic interactions at the top of the coral reef . Coral Reefs. 32. 10.1007/s00338-012-0976-y.

McCauley, D. J., Young, H. S., Dunbar, R. B., Estes, J. A., Semmens, B. X., & Micheli, F. (2012). Assessing the effects of large mobile predators on ecosystem connectivity. Ecological Applications, 22(6), 1711–1717. doi:10.1890/11-1653.1

Polanco, A; Acero, A. 2019. Biodiversidad de peces marinos del Caribe colombiano. La pesca en Colombia: del agua a la mesa. Agenda del mar p.23-27

Previero, M., & Gasalla, M. A. (2018). Mapping fishing grounds, resource and fleet patterns to enhance management units in data-poor fisheries: The case of snappers and groupers in the Abrolhos Bank coral-reefs (South Atlantic). Ocean & Coastal Management, 154, 83-95.

Pratt, H. L., Pratt, T. C., Morley, D., Lowerre-Barbieri, S., Collins, A., Carrier, J. C., … Whitney, N. M. (2018). Partial migration of the nurse shark, Ginglymostoma cirratum (Bonnaterre), from the Dry Tortugas Islands. Environmental Biology of Fishes, 101(4), 515– 530. doi:10.1007/s10641-017-0711-1

Puentes, V., Escobar, F. D., Polo, C. J., & Alonso, J. C. (2014). Estado de los Principales Recursos Pesqueros de Colombia–2014. Serie Recursos Pesqueros de Colombia–AUNAP. Oficina de Generación del Conocimiento y la Información, Autoridad Nacional de Acuicultura y Pesca–AUNAP

Ramírez, J. G., Lleonart, J., Coll, M., Reyes, F., & Puentes, G. M. (2017). Improving stock assessment and management advice for data-poor small-scale fisheries through participatory monitoring. Fisheries Research, 190, 71-83.

Reef guide.org Florents guide to the Florida, Bahamas & Caribbean reefs https://reefguide.org/carib/index1.html

Roff, G., Doropoulos, C., Rogers, A., Bozec, Y.-M., Krueck, N. C., Aurellado, E., … Mumby, P. J. (2016). The Ecological Role of Sharks on Coral Reefs. Trends in Ecology & Evolution, 31(5), 395–407. doi:10.1016/j.tree.2016.02.014

Salas, S., Chuenpagdee, R., Charles, A. T., & Seijo, J. C. (Eds.). (2011). Coastal fisheries of Latin America and the Caribbean (Vol. 544). ^ eRome Rome: Food and Agriculture Organization of the United Nations.

Sánchez-Jabba, A. M. (2012). Manejo ambiental en Seaflower, Reserva de Biosfera en el Archipiélago de San Andrés, Providencia y Santa Catalina. Documentos de Trabajo Sobre Economía Regional y Urbana; No. 176.

Sánchez, J. A., Gómez-Corrales, M., Gutierrez-Cala, L., Vergara, D. C., Roa, P., González- Zapata, F. L., ... & Sarmiento, A. (2019). Steady decline of corals and other benthic organisms in the SeaFlower Biosphere Reserve (Southwestern Caribbean). Frontiers in Marine Science, 6, 73.

Schmeller, D.S., Weatherdon, L.V., Loyau, A., Bondeau, A., Brotons, L., Brummitt, N., Geijzendorffer, I.R., Haase, P., Kuemmerlen, M., Martin, C.S., Mihoub, J.-B., Rocchini, D., Saarenmaa, H., Stoll, S., Regan, E.C., 2017. A suite of essential biodiversity variables for detecting critical biodiversity change. Biol. Rev. http://dx.doi. org/10.1111/brv.12332

Shideler, G. S., & Pierce, B. (2016). Recreational diver willingness to pay for goliath grouper encounters during the months of their spawning aggregation off eastern Florida, USA. Ocean & Coastal Management, 129, 36-43

Simcock, A. (2017). World Ocean Assessment. Cambridge University Press.

Speed, C. W., Cappo, M., & Meekan, M. G. (2018). Evidence for rapid recovery of shark populations within a coral reef marine protected area. Biological Conservation, 220, 308– 319. doi:10.1016/j.biocon.2018.01.010

Stevens, M. H. (2018). Bioeconomic Consequences of Fisheries Management: Florida's Commercial Reef Fisheries (Doctoral dissertation, University of Miami).

Teh, L. S., Cheung, W. W., Christensen, V., & Sumaila, U. R. (2017). Can we meet the Target? Status and future trends for fisheries sustainability. Current opinion in environmental sustainability, 29, 118-130.

Valdivia, A., Cox, C. E., & Bruno, J. F. (2017). Predatory fish depletion and recovery potential on Caribbean reefs. Science advances, 3(3), e1601303.

VLC media player VideloLan organization https://www.videolan.org/vlc/index.es.html.

Whitmarsh SK, Huveneers C, Fairweather PG. 2018 What are we missing? Advantages of more than one viewpoint to estimate fish assemblages using baited video.R. Soc. open sci. 5: 171993. http://dx.doi.org/10.1098/rsos.171993

Winter H.V & de Graaf M 2019 Diversity, abundance, distribution and habitat use of reef- associated sharks in the Dutch Caribbean

Worm, B., Davis, B., Kettemer, L., Ward-Paige, C. A., Chapman, D., Heithaus, M. R., Kessel, S. T., et al. (2013). Global catches, exploitation rates, and rebuilding options for sharks. Marine Policy, 40, 194–204. doi:10.1016/j.marpol.2012.12.034

Worm, B., Barbier, E. B., Beaumont, N., Duffy, J. E., Folke, C., Halpern, B. S., ... & Sala, E. (2006). Impacts of biodiversity loss on ocean ecosystem services. science, 314(5800), 787- 790.