Reef fish community in presence of the lionfish (Pterois volitans) in Santa Marta, Colombian Caribbean
Comunidad de peces arrecifales en presencia del pez león (Pterois volitans) en Santa Marta, Caribe colombiano
Rocío García-Urueña,1* Ph.D, Arturo Acero P,2 Ph.D, Víctor Coronado-Carrascal,1 B.Sc.
1Universidad del Magdalena, Grupo de Investigación Ecología y Diversidad de Algas Marinas y Arrecifes Coralinos. Carrera 32 # 22-08, Santa Marta, Colombia.
2Instituto de Estudios en Ciencias del Mar (CECIMAR). Universidad Nacional de Colombia sede Caribe, El Rodadero, Santa Marta, Colombia.
Received: October 2014; Acepted: March 2015.
Objetive. Fish species community structure and benthic organisms coverage were studied in five localities in Santa Marta where the lionfish is present. Materials and methods. Abundance of fish species, including lion fish, was established using 30 m random visual censuses and video transects; trophic guilds were established according to available references. On the other hand benthic coverage was evaluated using the software Coral Point Count (CPCe) 4.0. Results. Families with higher species numbers were Serranidae, Labridae, and Pomacentridae. Lionfish abundances were low (2.6±2.1 ind/120 m2), but in any case Pterois volitans was observed as the eleventh more abundant species, surpassing species of commercial value such as Cephalopholis cruentata. Species that were found in larger numbers (>100, Thalassoma bifasciatum, Haemulon aurolineatum, Canthigaster rostrata, Abudefduf saxatilis, Chromis cyanea, and Stegastes partitus) were mainly invertebrate eaters, planctivores, and territorial herbivores. Coral coverage showed higher coral percentages in Chengue (69.9%) and Cinto (27.4%), larger sponge percentages in Morro (32.7%); Isla Aguja and Remanso showed the larger figures for abiotic substrate (41.6 and 37%, respectively); corals, sponges, and gorgonians were the components best explaining fish community, but not for the lion fish, which inhabit all studied reef formations. Conclusions. Lion fish is ranked between the 20 more abundant species, with none commercially important species larger, hence no species may qualify as a natural control. Lion fish has as well become a relatively abundant species in Santa Marta reefs, independent of benthic coverage.
Key words: Exotic species, marine ecology, marine fishes (Source: IEDCYT).
Objectivo. Se estudió la estructura de especies de la comunidad íctica y se evaluó la cobertura de organismos bentónicos en cinco localidades en Santa Marta, Colombia con presencia del pez león. Materiales y métodos. Se estimó la abundancia a través de censos visuales y video transectos de 30 m y se estableció el gremio trófico de cada especie según literatura. El sustrato se cuantificó con el software Coral Point Count (CPCe) 4.0. Resultados. Las familias con más especies fueron Serranidae, Labridae y Pomacentridae y, aunque su abundancia promedio fue baja (2.6±2.1 ind/120 m2), Pterois volitans fue la undécima especie más abundante, superando a peces comerciales como Cephalopholis cruentata. Las especies más abundantes fueron invertívoros, planctívoros y herbívoros, tales como Thalassoma bifasciatum, Haemulon aurolineatum, Canthigaster rostrata, Abudefduf saxatilis, Chromis cyanea y Stegastes partitus. Se encontró mayor porcentaje de coral en Chengue (69.9%) y Cinto (27.4%) y de esponjas para Morro (32.7%); para Isla Aguja y Remanso predominó el componente abiótico (41.6 y 37%, respectivamente). Corales, esponjas y gorgonias fueron los componentes que mejor explicaron la comunidad íctica, aunque no para el pez león que habita todas las formaciones arrecifales. Conclusiones. El pez león se ubica entre las 20 especies de peces más abundante, con ninguna especie de importancia comercial en los sitios muestreados que lo supere en talla y que pudiera ser un control natural del invasor. Igualmente, se ha convertido en una especie relativamente abundante en los arrecifes samarios sin importar los atributos del fondo.
Palabras clave: Ecología marina, especies exóticas, peces marinos (Fuente: IEDCYT).
Since the mid-1970s, Acero y Garzón (1) have gathered information on the biodiversity of marine fish in the Santa Marta area, recording 372 species. Later, Acero (2) listed commercial species present in the Caribbean region of continental Colombia, citing a total of 449 species. These records are greatly relevant since they show the high number of species from the Lutjanidae, Serranidae, Carangidae, Haemulidae and Scaridae families.
To evaluate the deterioration of populations, Grijalba-Bendeck et al (3) analyzed different fishing techniques and disembarking points to determine priority species and conservation areas. Lutjanus analis and Mycteroperca interstialis were catalogued as vulnerable, and Epinephelus striatus as in danger of extinction. The most important factors that led to this condition were overfishing, deterioration, pollution, anthropogenic habitat alterations, and fishing below the minimum size for sexual maturity. In 2013 Álvarez et al (4) mentioned that fishing with increasingly more effective and less selective methods in the reefs of the Caribbean region of Colombia have meant that carnivorous fish have reached very critical levels where species such as Serranidae (groupers Epinephelus spp., Mycteroperca spp. and Cephalopholis spp.), Lutjanidae (snappers Lujtanus spp.) and Centropomidae (snooks Centropomus spp.) have practically disappeared or have been greatly reduced.
This problem has worsened with the recent lionfish (Pterois volitans) invasion. This species, native to the Indo-Pacific region, has become established with remarkable success in the western Atlantic Ocean, including the Caribbean Sea (5,6). Presently, a greater biomass and density has been recorded in the invaded area than with the nine lionfish (Pterois volitans) species occurring in their original distribution area (7,8). Apparently, this fish has devastating effects on native communities and could be one of the most harmful marine invasions that has ever been recorded (9). It is considered that in as little as five weeks P. volitans is capable of reducing the recruitment of native fish in small areas (5) by 80%, possibly affecting species that fulfill important ecological roles, such as herbivores (e.g Labridae and Pomacentridae). Similarly, this species could compete for food and space with other species that are economically important, such as snappers (Lutjanidae) and groupers (Serranidae), diminishing quantities and recruitment (5,7,10). Presently, the lionfish is considered worldwide as one of the 10 species that has the greatest ecological and economic impact on invaded sites (11).
In the Caribbean region of continental Colombia, González et al (12) were the first to document the presence of lionfish in the Tayrona National Park (Parque Nacional Natural Tayrona, PNNT), and since then the numbers of this fish have increased dramatically. In Colombia, it is considered that the invasion could contribute even further to reducing fish populations in the region, and even more so because a large number of variables make the problem even more complex (3,4). The objective of this study was to evaluate the composition in the fishing community and the availability of substrate both for the invading species as well as the native reef species in order to provide information that can be used as a reference for possible changes in the structure of the fish community, if there are any.
MATERIALS AND METHODS
Area of study. Five reef formations were studied: one located in the Santa Marta bay (Morro), another at the limit of Taganga Bay and Tayrona National Park (TNP) (Remanso), and three in the TNP (Isla Aguja, Chengue, and Cinto). Morro is at 11°14’N and 74°14’W, and its waters are constantly polluted from several sources: Boquerón (sewage water from the city), seaport (port and industry wastes), and Manzanares River (sediment and domestic waste), so that the reef patches only cover 20 to 28% (13).
Remanso, located at 11°16’N and 74°12’W, is at the extreme northeast of Taganga, with a primarily rocky shore and a shallow bordering reef (14). Geological formations on Isla Aguja (11°19’N, 74°12’W) are rocky-coral substrate, with an average depth of 25 m and a reef that is slightly inclined, of compact rock and stones (14). Chengue is a bay that is located in TNP at 11°19’N and 74°08’W, 14 km northeast of Santa Marta. The topography is heterogeneous, with a slight slope where patchy reefs are formed at a certain distance from the shore (13). The bay of Cinto is found at 11°20’N and 74°03’W, and is the central part of the marine sector of TNP. Exposure to waves in this area is similar to Chengue, and both bays have predominantly clear water.
Field methods. In each locality, a permanent transect 30 m long and 4 m wide (120 m2) and between 10 and 12 m deep was marked off; between January and December 2012 the number of lionfish was recorded monthly. The fish population was recorded three times during the study period. Using scuba diving equipment, two observers performed visual census for 30 minutes, counting individual fish from all the species found. Relative quantity analysis was considered as the relationship between the number of individuals of a species and the total of all species; in the same way, the relative number of families was determined by comparing its dominance in each locality. For each species, a trophic group was established through bibliographic revisions (carnivore, invertivore, planktivore, and herbivore), (15-17).
Benthic coverage of each transect was evaluated by video in each locality, and later 30 images were frozen and assigned 50 numbers at random. The substrate was classified according to the following components (coral, gorgonian, sponges, macroalgae, dead coral, hard substrate, and unidentified). To perform this analysis the software Coral Point Count (CPCe) 4.0. was used. Finally, the species richness and Shannon-Wiever diversity indexes (H’) and equitability (J) were calculated for each locality.
Data analysis. The distribution pattern of fish species was determined using the Bray-Curtis classification index (data transformed to square root) and multidimensional scaling using the abundance matrix for each locality. To establish possible associations between the composition of substrate and abundance in the fish community, exploratory analysis of substrate components was performed and the maximum correlation was determined (Bioenv). Later, a DistLM was performed (lineal model based on distance) that included those variables that presented the highest coefficients; this test helps discover models among the fish community using environmental variables of substrate components that describe significant correlations. The analysis was done using the Primer 6 statistics program, version 6.1.13.
A total of 88 fish species corresponding to 32 families were identified (Table 1). Of these, those that presented the greatest number of species were Labridae (14), Serranidae (9), Pomacentridae (8), and Haemulidae and Chaetodontidae (5). Out of all the species, 15 (17%) were found in all five localities, 4 (4.5%) were exclusive from Morro and Remanso, 8 (9.1%) from Isla Aguja, 9 (10.2%) from Chengue and 3 (3.4%) from Cinto. The greatest number of species and the greatest richness, uniformity and diversity were found in Isla Aguja. Although Chengue and Cinto bays had a similar number of species (50 and 49, respectively), there was a greater diversity (H’=3.33) and uniformity (J=0.85) in Chengue. Morro and Remanso showed similar values in the three indexes (Table 1).
Of the twenty most abundant species in all five localities (#ind./120 m2), those that showed higher values were Thalassoma bifasciatum and Abudefduf saxatilis with 48 and 47 individuals. They were followed by Chromis cyanea, Clepticus parrae, Stegastes partitus, Haemulon aurolineatum, and Canthigaster rostrata with abundances between 22 and 32 individuals. Pterois volitans was found with an average abundance per transect of 9.8 ind./120 m2 which place it in 11th place (Figure 1).
According to their feeding habits, invertivore species predominated (45.1%), the most abundant being T. bifasciatum, C. rostrata, and H. aurolineatum. Carnivore species followed in importance (24%); in this case, P. volitans was the most abundant species in this group, along with Cephalopholis cruentata. Herbivores came in third place (18%), S. partitus and Sparisoma chrysopterum were the most abundant. Lastly, planktivores (12.1%) with A. saxatilis and C. cyanea. As for localities, Remanso presented the greatest percentage of invertivore, herbivore, and planktivore groups (50%, 22.5%, and 15% respectively). Carnivores were the most abundant in Cinto bay (32.7%) (Figure 2).
Relating to substrate, a greater percentage of coral coverage was found in Chengue (70%), followed by Cinto (27%), and Isla Aguja (24%). The presence of gorgonias was higher in Remanso (37%) and Morro (32%). In Cinto macroalgae predominated (47%); and the abiotic substrate was greater in Remanso (41%) and Isla Aguja (37%). The rest of the components were variable for each locality with percentages greater than 15% (Figure 3).
The fish community in Chenque bay is distinct from the rest of the reef formations both in the exploratory analysis (Bioenv, DistLM) (Figure 4) as well as in the Bray-Curtis dendrogram of similarity. Groups that were defined as similar were in Morro and Isla Aguja (55%) and Remanso and Cinto (52%) (Figure 5). Corals, gorgonias and sponges were the substrate component variables that best related to the abundance in the fish community, with a correlation of 0.806. 33% of the variation is explained in Chengue by associating corals and sponges, while in Morro and Remanso with abiotic substrate (Figure 4).
For Gaira bay (3 km southeast of the Santa Marta bay) Grijalba-Bendeck et al (18) evaluated fish through the technique of stationary visual census and the results showed that families Serranidae, Lutjanidae, Labridae and Scaridae [(presently included in Labridae (19)] were the most abundant. Evaluating fish associated to coral formations in the Caribbean region of Colombia, specifically Chengue, Reyes-Nivia et al (20) showed the importance of families Serranidae, Scaridae [(presently included in Labridae (19)], Labridae, Pomacentridae, Haemulidae, Lutjanidae, and Gobiidae; Olaya-Restrepo et al (21) evaluated the catch of reef fishes in 20 stations near Santa Marta and TNP and showed that families Serranidae, Haemulidae, Gobiidae, Scaridae [(presently included in Labridae (19)] and Pomacentridae as the most dominant.
In general terms, and as shown in this study, the abundance of families Serranidae, Haemulidae, and Labridae is constant; however, family Lutjanidae, that was believed important did not appear as such in Olaya-Restrepo et al (21). Nevertheless, family Gobiidae, which is usually well represented, was not recorded; this could be due to the methods and purposes previously used, since, in this case, cracks and rifts were not examined during the census, and large areas and different depth strata were not covered.
Regarding species numbers, Acero and Garzón (1) list 372 species from the Santa Marta region, considering it as being biologically rich. This document is a starting point for comparing the present state of the fish fauna in the region. For example, Grijalba-Bendeck et al (18) mentioned that 30% of the previously mentioned species were recorded in Gaira; additionally, those belonging to the Serranidae family were found in reduced numbers, which the authors attributed possibly to overfishing. Reyes-Nivia et al (20) list 149 species in Chengue, with commercially important fish of the families Serranidae and Lutjanidae, such as Mycteroperca acutirostris, M. bonaci, M. interstitialis, M. tigris, M. venenosa, Lutjanus analis, L. griseus, and L. jocu, none of which were seen in this study.
Chengue bay, where mangrove, marine grass and reef patches are present but were not evaluated because reef formation monitoring was already established in its central area; the species listed (50 species) were less than those found by Olaya-Restrepo et al (21) (between 62 and 95 species). However, Lutjanus cyanopterus was recorded, a piscivorous species that could play an important role in the control of lionfish, even more so since, as previously mentioned, no other species that could compete or prey on the invader was seen.
Olaya-Restrepo et al (21) studied 20 stations showing an average diversity index of 1.73 in TNP and 1.68 in unprotected areas; four localities coincide with this study and the results generally show a greater number of species (70 in Morro, 62 in Isla Aguja, 62 and 95 in Chengue and between 70 and 80 in Cinto), although commercially important fish such as Mycteroperca tigris, M. venenosa, M. phenax, Epinephelus guttatus, E. itajara, Lutjanus analis and L. buccanella were not recorded. Additionally lower averages for individuals and much lower densities were found in large snapper and grouper species; only L. mahogoni was abundant in the TNP protected area and Cephalopholis cruentata in unprotected stations.
In comparison with that study, L. mahogoni, in spite of being observed in the park, only had a relevant abundance in Chengue, and C. cruentata, which was present in the five localities, was more abundant in those outside of TNP. In spite of being considered a protected area, Isla Aguja is visited daily by tourists and fishermen; it was the reef formation that had the greatest richness and diversity of species (54 species and H’=3.49) and that, along with Chengue and Cinto, presented the highest diversity values. Krajewski and Floeter (17) mentioned the protected marine areas as an important factor that can influence the differences in fish communities. Their study compared protected and uninhabited fishing sites with a marine park that permits local fishing, and it was found that the main species that interest fishermen were the macrocarnivores, so that the great predatory fish in the trophic chain were less abundant. In the Santa Marta region, it has been determined that important carnivore species have been diminishing (18,20,21), which could have had an effect on the proliferation of the invading species.
The structure of the fish community is due to biotic variables such as the abundance of potential competitors (22) and prey (15). In this case, with the presence of the invader, Maljkovic et al (23) found that in the Bahamas M. tigris and E. striatus preyed on the lionfish. Mumby et al (24), in the same region, studied a group of groupers, such as E. striatus, M. tigris, M. bonaci, M. venenosa and M. interstitialis, founding a seven fold lineal reduction in the lionfish biomass in relation to groupers; therefore, evidence suggests that predators can play a role as natural control. In this study, the rarity or absence of mid-sized piscivore can impact the proliferation of the invading species, which is the most abundant predatory fish, even above the small carnivores that are not actively sought by fishermen; this hypothesis should be evaluated in future studies.
In terms of species composition in reef formations where lionfish is present, Lesser and Slattery (25) studied a reef in the Bahamas between 2003 and 2009 with phase changes in communities at mesophotic depths in which, as herbivore fish diminished due to the presence of lionfish, the areas became dominated by algae. The study shows how, under invader presence and its depredation, 19 species were utilized with the consequent reduction of herbivore, planktivore, and spongivore species as well as those that feed on small crustaceans. This impact is called cascade, whether directly due to the consumption of herbivores or indirectly due to species displacement.
The study performed by Morris and Akins (26) mentioned that the lionfish diet is diverse, feeding mainly on small fish that are equally important for many commercially important species such as Serranidae and Lutjanidae. Regarding the analysis of the stomach content of lionfish in North Carolina, Muñoz et al (27) suggested a general carnivore diet made up of 3.8% crustaceans, cephalopods, bivalves and ophiuroids, and the rest composed by 16 fish families, the most abundant being Haemulidae, Labridae, and Serranidae. In the Colombian Caribbean, lionfish diet was initially analyzed by Muñoz-Escobar and Gil-Agudelo (28) and it was likewise identified as a generalist carnivore, with the family Serranidae being the most predominant. Also, species of the families Gobiidae, Clupeidae, and Pomacentridae that, although have little or no commercial importance, are part of the diet of Lutjanidae and Haemulidae, which are commercial families that have diminished their abundances in recent years.
Muñoz et al (27) mentioned that the lionfish diet would be determined according to prey availability. In our study, although the results showed that carnivore, invertivore and herbivore species were predominant, they had low abundances. Thus, in analyzing the 20 most abundant species, planktivores and invertivores were better represented. More than half (70%) of the fish abundance in the Santa Marta region was composed of ten species. Of these, three are invertivores, four are planktivores, and three are herbivores, ingesting plankton and small invertebrate and algae; those ten species are smaller than the lionfish and, due to their abundance, could have become prey too and influenced the proliferation of the invader (28). It is clearly indicative of the overexploitation of fish resources in the Santa Marta region that the invader quickly became one of the most abundant species and the most important fish predators.
Whitfield et al (29) compared the abundance of lionfish with groupers between 35-50 m deep and between 50 and 100 m in North Carolina. Lionfish was found with average abundance at 21.1 ind/ha in shallow areas and 5.2 ind/ha in deep waters, and in both depths it was observed second in abundance, after Mycteroperca phenax. Unfortunately, there is no starting point recorded in 2008 and 2009, which is when lionfish appeared in Colombian waters (6, 12). In general, no records show the Scorpaenidae family as significant in abundance or biomass in the Colombian Caribbean. Now, under lionfish presence, it was observed to be even more important than species such as C. cruentata, which was the only one observed among the twenty most abundant species and no grouper of considerable size was observed in the sampled sites that could act as a natural control for the invader.
According to Munday et al (30) and Gardiner and Jones (31), some types of sustrate, such as corals and sponges, can be used as feeding sites or refuge, and these can influence fish community structure. For example, strong correlations have been found between substrate composition and reef fish with specialized diets densities (e.g. butterflyfish and angelfish) and with habitat requirements (gobies and some cardinalfish) (15). When analyzing density of fish biomass, Krajewski and Floeter (17) found a positive correlation with coral coverage, depth and areas protected from waves, where mobile carnivores and invertivores were more influenced by unconsolidated bottoms and substrates, planktivores and omnivores by wave exposure, and herbivores by algae coverage, with the existence of general habits that suggest that the community is dominated by versatile species.
Substrate components such as corals and sponges in Chengue bay, and the abiotic substrate in Morro and Remanso, were the variables that best explained fish composition. Association of lionfish to substrate was only evident in Chengue and Morro, localities where the invader was more abundant. It should be kept in mind that in tropical systems positive relationships between coral coverage and fish density and biomass have been considered as indicators of the complexity of the habitat by offering more shelter for medium-sized fish (between 10 and 40 cm LT) (17); results show that, while lionfish was more abundant in areas with greater coral coverage, sponges, or abiotic substrate, it has also occupied many other habitats. However, detailed studies need to be performed that discriminate the availability of food, fish composition by locality, and different associated substrates and ecosystems to determine the possible effects on the community.
To Luis Manjarrés Martínez for his support with statistical analysis. To the proposal funded by Fonciencias and the Universidad del Magdalena “Invasión del pez león Pterois volitans registro de sus abundancias, estructura de tallas y preferencia al sustrato en Santa Marta, Caribe colombiano,” and to the proposal “Invasión del pez león a los arrecifes del Caribe colombiano: biología, ecología y origen” funded by Colciencias (1361-521-28271).
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