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Record of abundance, spatial distribution and gregarious behavior of invasive lionfish Pterois spp. (Scorpaeniformes: Scorpaenidae) in coral reefs of Banco Chinchorro Biosphere Reserve, southeastern Mexico.

The invasion of lionfishes (Pterois volitans, P. miles) is considered one of the greatest threats to biodiversity in the Atlantic Ocean (Hixon et al., 2016). In three decades, lionfishes invaded and settled in the eastern coasts of the United States, the Caribbean Sea, the Gulf of Mexico and the southeastern coast of Brazil (Cote & Smith, 2018), reaching higher densities than in its native area (Darling et al., 2011; Kubicki et al., 2012). Its presence in reefs has caused ecological impacts triggering a decrease in the density and biomass of native fishes (Albins, 2015), and competing for space and food with species of a similar trophic level (Albins, 2013). The direct effects of the lionfish could be combined with other stressors such as overfishing and pollution in Caribbean reefs (Albins & Hixon, 2013), resulting in a biodiversity crisis.

In Banco Chinchorro, Mexico, the first lionfish (14 cm total length) was captured by a fisherman nearby Cayo Centro area, at 3 m water depth on 9 July 2009. However, it is very likely that the invasion had begun years before the first sighting (Sabido-Itza et al., 2016b). The impacts of the rapid population establishment on Mexican coasts is just beginning to be understood (Garcia-Rivas et al., 2018).

The objectives of this study are to describe the abundance (density and biomass), spatial distribution, size structure, and gregarious behavior of the lionfishes in Banco Chinchorro Biosphere Reserve (BCBR). "Lionfish" and Pterois spp. refer to both species, due to the recent record of P. miles in BCBR (Guzman-Mendez et al., 2017). This Marine Protected Area is considered a priority in the Mesoamerican Reef System region, so the results presented here are important to determine the course of monitoring and control efforts.

The Chinchorro reef system is in the southeastern of the Yucatan Peninsula, Mexico (18[degrees]47'-18[degrees]23'N, 87[degrees]14'-87[degrees]27'W) (Carricart-Ganivet & Beltran-Torres, 1998), 30.8 km away from the mainland and separated from the coast by a 1,000 m deep channel (Fig. 1).

In order to estimate the abundance and distribution of the lionfish in the reefs of BCBR, four sites were monitored (4, 5, 8 and 10) in 2012, and 22 sites in 2013 from March to May between 09:00 h and 12:00 h. Depending on the depth and sea conditions, between four and six visual censuses of 30 m length and 4 m width were performed, deployed parallel to the main reef formation at each site. To avoid bias in the detection of lionfish, two people trained in monitoring performed censuses. Each diver did a thorough search in cavities, overhangs, cracks and any potential habitat, recording the total number of lionfishes in each transect, visually estimating the size of all fishes to the nearest centimeter and its gregarious behavior. This methodology was adapted from that proposed by Green et al. (2013).

The recorded lengths of the lionfishes were converted to weight using the length-weight relationship parameters (a = 0.0042, b = 3.258), obtained from Sabido-Itza et al. (2016a). The biomass was estimated as the sum of fish weights recorded in a transect. A t-test was used to determine differences in density and biomass between years and a Simple Variance Analysis (ANOVA) was used to determine statistical differences in density and biomass between sites and distribution zones in 2013, followed by a post-hoc LSD-Fisher test.

The data were transformed to log (x + 1), due to a large number of zeros found in transects. The normality and homogeneity of variance were tested by the Shapiro-Wilks and Levene's tests, respectively. The lengths and weights were evaluated by zone using the t-test.

Lionfish groups were classified into four categories: lone individual, group of two, group of three and group of [greater than or equal to]4 fish. The number of lionfishes showing some grouping ([greater than or equal to]2 organisms) among the total recorded fish, resulted in the relative gregarious behavior. Finally, the mean cluster size (# fish) was obtained among the total groupings observed.

Four sites were monitored on the leeward side to compare densities and biomass between 2012 and 2013, and we found that in 2013 the densities were 1.9 times greater than in 2012 (75.36 [+ or -] 106.70 vs 147.73 [+ or -] 166.53) and biomass was similar (18.86 [+ or -] 27.93 vs 20.42 [+ or -] 27.02). However, no significant difference was found between years (t = -0.72, P = 0.47 and t = 0.76, P = 0.45).

At the 22 sites monitored in 2013, the average density and biomass (mean [+ or -] SD) found in BCBR was 97.58 [+ or -] 140.25 ind [ha.sup.-1] and 18.20 [+ or -] 29.88 kg [ha.sup.-1] respectively (Table 1). At the sites, significant differences were found between densities (ANOVA: [F.sub.21,92] = 2.6, P < 0.001) and biomass (ANOVA: [F.sub.21,92] = 2.6, P < 0.001).

There was a marked difference in density and biomass of Pterois spp. at sites located in the leeward reefs (LR) with respect to those located in the windward reef (WR), (ANOVA: [F.sub.1,115] = 30.01, P < 0.000 and ANOVA: [F.sub.1,112] = 23.29, P < 0.000 for density and biomass respectively). LR mean density was 4.6 times higher than WR (154.57 [+ or -] 163.8 vs 33.33 [+ or -] 63.3 ind [ha.sup.-1]). The mean biomass was 3.9 times higher in LR than WR (28.42 [+ or -] 35.0 vs 7.25 [+ or -] 17.8 kg [ha.sup.-1]) (Figs. 2a-2b).

Total length ranged from 5 to 40 cm (23.4 [+ or -] 9 cm), while weight ranged from 0.8 to 696.4 g (188.2 [+ or -] 179.3 g). Because no difference was found between LR and WR sizes (t = 0.25, P = 0.80), total lengths were all grouped into a histogram (Fig. 3). From the total number of observations, 47.5% of the lionfishes presented some sort of aggregation. Finally, the number of groups of lionfishes was higher in LR (24) than WR (2) (Table 2).

Data collected in this study confirm the settlement and wide distribution of Pterois spp. on the reefs of the BCBR, Mexico. The lionfish densities and biomass are higher than in their native environment, confirming previous results of comparisons for other invaded areas (Darling et al., 2011; Kulbicki et al., 2012).

Densities reported here can be considered as intermediate, within the invaded range, because sites with densities below 50 ind [ha.sup.-1] and sites above 300 ind [ha.sup.-1] have been recorded (Table 3). Sites with high densities (>300 ind [ha.sup.-1]), may present significant negative changes in the native reef-fish community (Albins, 2015).

Biomass in BCBR was very similar to that found in New Providence, in the Bahamas, with 19.2 [+ or -] 29.3 kg [ha.sup.-1]. Nevertheless, it was 6 to 12 times higher than that found in San Salvador Island and Kenya with 2.7 and 1.5 kg [ha.sup.-1], respectively (Darling et al., 2011; Anton et al., 2014). The wide variety of density and biomass records reported here and in the Atlantic Ocean may be related to factors characteristic of the biogeographic region (Hackerott et al., 2013; Cure et al., 2014), the year of the first report and subsequent monitoring (Cobian-Rojas et al., 2016), habitat (Lesser & Slattery, 2011; Anton et al., 2014; Bejarano et al., 2015), or the methodology used in sampling (Green et al., 2013; Tilley et al., 2016).

The location of sites in BCBR, relative to wave exposure, had a great influence on the values of the density and biomass of Pterois spp. Chollett & Mumby (2012) mentioned that the winds in the region are predominantly northeastern, dominating the patterns of wave exposure, i.e., causing fewer waves on the leeward side than in the windward direction. Lack of wave exposure in LR favors the presence of lionfish while the higher waves inhibit their hunting functions (Anton et al., 2014; Garcia-Rivas et al., 2018). Also, LR is likely to serve as a feeding ground for lionfishes, due to the high abundance of reef fish recruits (Villegas-Sanchez et al., 2015). Ocean currents can also play an important factor. On the western flank on the BCBR, the currents usually move south (anticyclonically) slowly, allowing for the retention and settlement of larvae (Carrillo et al., 2015).

Sizes and weights found in the BCBR are like that of various regions in the Atlantic Ocean (Sabido-Itza et al., 2016b; Chapman et al., 2016; Cobian-Rojas et al., 2016). Rapid growth rates (Cote & Smith, 2018) and high prey consumption have helped to achieve greater lengths than those found in its natural range (Darling et al., 2011). In our study, about 65% of the organisms were considered sexually mature, i.e., the population is dominated by adults (Gardner et al., 2015).

Finally, it has been reported that in their natural habitat (Cure et al., 2014; McTee & Grubich, 2014) and in the Atlantic Ocean (Agudo & Klein-Salas, 2014: Garcia-Rivas et al., 2018), the herding behavior of the lionfish is common. In Venezuela, gregarious behavior was reported for 44% of the individuals, whereas in the Philippines and Guam in the Pacific Ocean was 54 and 26% respectively (Agudo & Klein-Salas, 2014; Cure et al.,2014). The average number of lionfishes found in groups in BCBR was less (2.5 ind) than that found in their native communities (4.9 and 3.8 ind) (Cure et al., 2014). Regarding survey areas, LR presents a major proportion of groups than WR. Ecologically, these aggregations serve to increase the success of hunting and reproduction, which can be more significant in LR due to the availability of potential preys and abundance of lionfish for possible mating (Garcia-Rivas et al., 2018).

Since the earliest records of lionfish specimens in Mexico, authorities have implemented actions such as fishing tournaments (Malpica-Cruz et al., 2016) and promoted its use for consumption (Carrillo-Flota & Aguilar-Perera, 2017) to try to reduce its abundance and the consequent impact on local ecosystems. In Banco Chinchorro, management is based on capture during fishing tournaments and by daily catch brigades for approximately five months with local anglers and tourist service providers. However, our results show that at least as of 2013, the abundance of lionfish has not diminished. Therefore, better planning is needed. Our recommendation is to promote lionfish extraction from leeward reefs in order to benefit and aid in the conservation of the native species that inhabit this area. This work serves to understand the distribution of the lionfish in the BCBR. Now, studies that focus on corroborating the environmental factors that determine the distribution of the lionfish, its impacts in the native reef-fish community and the efficacy of ongoing removals in the Mexican coasts are required.

ACKNOWLEDGMENTS

We thanks the GEF/Small Grants Programme for the financial support provided by the project MEX/SGP/OP5/FSP/STAR/BD/13/51. To the National Commission of Natural Protected Areas (CONANP), to the Banco Chinchorro Biosphere Reserve, to its assigned personnel, especially Jose Dominguez-Calderon, Yareni Perera-Romero and Angel Moreno-Beltran. Likewise, this work would not have been possible without the support of the fishermen of the three fishing cooperatives, in particular, Emiliano Martinez, Miguel Jarillo, Manuel Frias, Erick Xicum, Jaime Medina and Didier Garcia. We thank Dr. Nuno Simoes for his accurate observations, Dra. Anastazia Banaszak for the English translation and Irving Chavez for helping in editing figures.

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Villegas-Sanchez, C.A., Lara-Arenas, J.H., Castro-Perez, J.M. & Arias-Gonzalez, J.E. 2015. Patrones de reclutamiento de 4 especies icticas en habitats de parche y cordillera del arrecife Banco Chinchorro (Caribe mexicano). Revista Mexicana de Biodiversidad, 86(2): 396-405.

Miguel Mateo Sabido-Itza (1) & Maria del Carmen Garcia-Rivas (2)

(1) Instituto Tecnologico de Chetumal, Maestria en Manejo de Zona Costera, Quintana Roo, Mexico

(2) Comision Nacional de Areas Naturales Protegidas, Parque Nacional Isla Contoy y Parque Nacional Arrecifes de Puerto Morelos, Puerto Morelos, Quintana Roo, Mexico

Corresponding author: Miguel Sabido-Itza (mateosabido@gmail.com)

Corresponding editor: Guido Plaza

Received: 8 September 2017; Accepted: 3 October 2018

DOI: 10.3856/vol47-issue2-fulltext-15
Table 1. Lionfish (Pterois spp.) density and biomass in monitored sites
in 2013 in Banco Chinchorro Biosphere Reserve (BCBR), Mexico. SD:
standard deviation.

Zone           Site                        2013
                       Density [+ or -] SD    Biomass [+ or -] SD
                        (ind [ha.sup.-1])       (kg [ha.sup.-1])

Leeward reef     1    125 [+ or -] 87.40      32.15 [+ or -] 23.11
                 2     20.83 [+ or -] 41.67    4.54 [+ or -] 9.08
                 3    152.78 [+ or -] 97.42   33.46 [+ or -] 31.94
                 4     83.33 [+ or -] 58.92   22.93 [+ or -] 14.28
                 5    222.22 [+ or -] 291.86  28.15 [+ or -] 42.46
                 6    145.83 [+ or -] 125     50.82 [+ or -] 57.46
                 7    333.33 [+ or -] 68.04   40.85 [+ or -] 32.81
                 8    152.78 [+ or -] 97.42    4.68 [+ or -] 4.04
                 9    291.67 [+ or -] 296.98  51.77 [+ or -] 53.80
                10    116.67 [+ or -] 95.01   27.54 [+ or -] 28.65
                11    166.67 [+ or -] 117.85  58.74 [+ or -] 41.20
                12     41.67 [+ or -] 69.72    0.61 [+ or -] 1.20
Windward Reef   13     20.83 [+ or -] 41.67    9.39 [+ or -] 18.78
                14     55.56 [+ or -] 68.04    6.99 [+ or -] 13.96
                15     13.89 [+ or -] 34.02    2.09 [+ or -] 5.12
                16      0                      0
                17     41.67 [+ or -] 45.64    0.92 [+ or -] 1.72
                18     41.67 [+ or -] 45.64   11.36 [+ or -] 12.45
                19     33.33 [+ or -] 74.54   12.78 [+ or -] 28.57
                20    100 [+ or -] 149.07     29.13 [+ or -] 41.07
                21     16.67 [+ or -] 37.27    4.54 [+ or -] 10.16
                22     13.89 [+ or -] 34.02    0.11 [+ or -] 0.26
               Total   97.58 [+ or -] 140.25  18.20 [+ or -] 29.88

Table 2. Gregarious behavior of lionfish Pterois spp. in Banco
Chinchorro Biosphere Reserve, Mexico. Data are presented as the total
number of registered fish (No fish), the number of solitary fishes, the
total number of registered groups, group number 2, 3 and from 4 to 7
fish and the average [+ or -] SD group size. n: number of fishes, %:
percentage of each group.

    No   Solitary  No groups  Groups of     Groups of    Groups of four
   fish              total    two fishes  three fishes  to seven fishes

n  137     72        26          18           6                2
%  100     52.5      47.5        26.3        13.1              8.1

       Mean group
          size

n  2.5 [+ or -] 1.1
%

Table 3. Densities of lionfish Pterois spp. reported in native and
invaded sites. SD: standard deviation.

Region   Locality                              Density

Native   Philippines                             Low
Native   Guam                                    Low
Native   Mombasa, Kenya                          Low
Native   Red Sea                                 Low
Native   Pacific Ocean                           Low
Native   Indian Ocean                            Low
Invaded  Island of San Salvador, Bahamas         Low
Invaded  Venezuelan coast                        Low
Invaded  South Caicos, Turks & Caicos Islands    Low
Invaded  Bacalar Chico, Belize                   Low
Invaded  New Providence, Bahamas               Medium
Invaded  Curacao                               Medium
Invaded  Bonaire                               Medium
Invaded  Little Cayman, Cayman Islands         Medium
Invaded  Lee Stocking Island, Bahamas           High
Invaded  Cape Eleuthera, Bahamas                High
Invaded  Guanahacabibes, Cuba                   High
Invaded  San Andres, Colombia                   High
Invaded  Banco Chinchorro, Mexico              Medium

Region   Media [+ or -] SD (ind [ha.sup.-1])  Source

Native            21.94 [+ or -] 6.5          Cure et al. (2014)
Native             3.53 [+ or -] 0.9          Cure et al. (2014)
Native            25.1 [+ or -] 45.7          Darling et al. (2011)
Native            24.1 [+ or -] 44.9          McTee & Grubich (2014)
Native             0.17                       Kulbicki et al. (2012)
Native             3.6                        Kulbicki et al. (2012)
Invaded           13 [+ or -] 18              Anton et al. (2014)
Invaded           25.83 [+ or -] 66.51        Agudo & Klein-Salas (2014)
Invaded           16.79                       Tilley et al. (2015)
Invaded           27.1 [+ or -] 8.8           Chapman et al. (2016)
Invaded          101.7 [+ or -] 103           Darling et al. (2011)
Invaded          127                          de Leon et al. (2013)
Invaded           66                          de Leon et al. (2013)
Invaded          162                          Bejarano et al. (2015)
Invaded          530 y 640                    Lesser & Slattery (2011)
Invaded          300 [+ or -] 600             Green et al. (2013)
Invaded          310                          Cobian-Rojas et al. (2016)
Invaded          379 [+ or -] 220             Gonzalez-Corredor et al.
                                              (2016)
Invaded           97.6 [+ or -] 140.2         This study
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Title Annotation:Short Communication
Author:Sabido-Itza, Miguel Mateo; Garcia-Rivas, Maria del Carmen; Plaza, Guido
Publication:Latin American Journal of Aquatic Research
Date:May 1, 2019
Words:3656
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