Bull Mar Sci. 92(2):181–190. 2016 research paper http://dx.doi.org/10.5343/bms.2015.1033
Density and depth distribution of the sympatric species Squilla chydaea and Squilla empusa (Stomatopoda: Squillidae) in the southern Gulf of Mexico
Departamento de Recursos Marco Antonio May-Kú * del Mar, Cinvestav, Carretera antigua a Progreso, km 6. Apdo. J Gabriel Kuk-Dzul Postal 73-Cordemex, 97310 Teresa Herrera-Dorantes Mérida, Yucatán, Mexico. Pedro-Luis Ardisson * Corresponding author email:
Stomatopods (order Stomatopoda), commonly known as mantis shrimps, are represented by 449 recorded species, 45 of which are found in the Gulf of Mexico (Reaka et al. 2009). Stomatopods prey on fishes, molluscs, annelids, and other invertebrates (Cronin et al. 2006), and are important food items for certain fishes, including commercially important species such as the red grouper, Epinephelus morio (Valenciennes, 1828) (Brulé and Rodríguez-Canché 1993). Some stomatopods have commercial value, such as Squilla mantis (Linnaeus, 1758) and Oratosquilla oratoria (De Haan, 1844), fished in the Mediterranean Sea and off Japan, respectively (Hamano et al. 1987, Maynou et al. 2004). Stomatopods can also serve as biological
Bulletin of Marine Science 181 © 2016 Rosenstiel School of Marine & Atmospheric Science of the University of Miami 182 Bulletin of Marine Science. Vol 92, No 2. 2016 indicators of petroleum hydrocarbons and heavy metals in the marine environment (Risk et al. 2001, Blasco et al. 2002). Campeche Sound, in the southern Gulf of Mexico, is an area of ecological and economic importance due to its high biodiversity and the ongoing exploitation of its natural resources, especially through petroleum extraction and shrimp fisheries (Soto et al. 2014). In this area, stomatopods of the family Squillidae are represented by six genera and 15 species. Five of these belong to the genus Squilla: Squilla chydaea Manning, 1962; Squilla deceptrix Manning, 1969; Squilla edentata edentata Lunz, 1937; Squilla empusa Say, 1818; and Squilla rugosa Bigelow, 1893 (Reaka et al. 2009). With regard to the western Atlantic Ocean, there is a wide body of literature that mentions the spatial distribution of some of these species—e.g., S. deceptrix, S. e. edentata, S. empusa, and S. rugosa (Holthuis 1959, Werding and Müller 1990, Tavares 2002, Reaka et al. 2009). However, in the southern Gulf of Mexico, patterns of spatial distribution and density of squillid stomatopods are poorly known. In Campeche Sound, information on this group comes from studies by Vázquez- Bader and Gracia (1994), Ruiz (2008), and Ruiz et al. (2013), which indicated that S. chydaea (nearly endemic to the Gulf of Mexico) and S. empusa (widely distributed in the western Atlantic Ocean) are the most abundant species of Squilla on the continental shelf. Squilla empusa has been recognized as a potential fishery resource in the Gulf of Mexico (Tavares 2002, Wortham 2009), but presently no stomatopod species are commercially exploited in this area, although they are frequently caught as bycatch by the industrial shrimp fleet and discarded at sea. Analysis of the spatial distribution of sympatric congeneric species is fundamental for understanding ecological relationships between coexisting populations and can inform proper management. The aim of the present study was to assess the population density and depth distribution of the sympatric stomatopods, S. chydaea and S. empusa, on the continental shelf of Campeche Sound during the rainy season. These data were obtained as part of an ongoing environmental monitoring program in the southern Gulf of Mexico.
Methods
Campeche Sound is located in the south-southwest sector of the Gulf of Mexico and forms part of the continental shelf situated between the Mexican states of Tabasco and Campeche. Campeche Sound covers approximatley 65,000 km2, with depths ranging from 0 to 200 m. The western part of the sound (Campeche Bay) re- ceives substantial inputs of organic material from river runoff, while the eastern part (Campeche Bank) receives a minimal level of continental influence and the sediments have high carbonate content (Hernández-Arana et al. 2005). Three weather seasons prevail in Campeche Sound: dry (March–May); rainy (June–October); and the sea- son of cold fronts or “nortes” (November–February). In the present study, sampling was conducted during only the rainy season months (July, August, and October) of 2012 and 2013. Sixty sampling sites were distributed across an area between 18°N–21°N and 91°W–93°W, with depths ranging from 6 to 170 m. These sites are part of the sampling grid of the Environmental Monitoring Program of the southern Gulf of Mexico, carried out jointly by PEMEX Exploración y Producción-Regiones Marinas and the Centro de Investigación y de Estudios Avanzados (Cinvestav) Unidad Mérida, an ongoing interdisciplinary program focused on understanding May-Kú et al.: Squilla stomatopods in Campeche Sound 183 the environmental condition of the southern Gulf of Mexico. A commercial shrimp trawl net with a mouth aperture of 14 m and 38-mm cod-end mesh size was used for collection of benthic fauna aboard the RV Justo Sierra from the Universidad Autónoma de México and the commercial shrimp vessel Campeche I. At each site, one bottom trawl was performed for 25–30 min at a mean trawling speed of 4345 m hr−1, and sweeping an area of about 2.5 ha. Otter trawls are commonly used for col- lection of benthic fauna, providing reliable quantitative estimates of population den- sity. However, they likely underestimate the density of some invertebrate taxa, such as stomatopods, due to their burrowing behavior (Syuhada 2011). Vessel time is ex- pensive; thus, the sites were visited at varying times throughout the day and night to maximize efficiency. In 2012, 22 sites were sampled during the day (06:00–18:00 hrs) and 4 at night (18:00–06:00 hrs), while in 2013, 23 and 11 sites were sampled during day and night, respectively. All benthic fauna collected were frozen at −20 °C and transported to the laboratory, where stomatopods were separated from other inver- tebrates and individually identified to species using the taxonomic keys of Manning (1969) and Manning and Heard (1997). For each stomatopod species, we used a two-way analysis of variance (ANOVA) to test whether density (ind ha−1) varied with year (2012, 2013) and sampling time (day, night). Density data were log-transformed [log (x+1)] prior to analysis to ful- fill ANOVA assumptions of normality and homogeneity of variance. When ANOVA test detected significant differences, post hoc comparisons among means were per- formed using Bonferroni test with corrected P value for the number of comparisons made (e.g., 0.1 / 6 = 0.016). To evaluate differences in depth distribution between S. chydaea and S. empusa, we used a Student’s t-test to test for differences in mean depth. This analysis was performed for each year separately. The relationship -be tween density and water depth, evaluated separately by stomatopod species and year, was analyzed using Poisson and negative binomial general linear models (NB1 and NB2 forms; i.e., linear negative binomial and quadratic negative binomial, respec- tively) in the R software package (R Development Core Team 2008). The best fitting model was selected on the basis of the smallest Akaike information criterion (AIC) value among the models tested (Akaike 1973). An alpha level of 0.1 was used as the criterion for statistical significance for statistical analyses. Statistical analyses were performed in the statistical package InfoStat version 2011 (Di Rienzo et al. 2011).
Results
During both years, we collected a total of 234 stomatopods, belonging to two Squilla species. Of these, 45% were S. chydaea and 55% were S. empusa (Table 1). In 2012, S. chydaea was present at 9 of the 26 sites, and in 2013, at 9 of the 34 sites. For this species, maximum densities were observed in 2012 during both day (8.4 ind ha−1) and night (6.8 ind ha−1) at two sites located offshore off Terminos Lagoon (19°32´N, 91°44´W, 41.5 m depth, and 19°33´N, 91°54´W, 55 m depth) (Fig. 1A,B). In 2012, S. empusa was present at 8 of the 26 sites, and in 2013, at 10 of the 34 sites. For this species, maximum densities were observed during night in 2012 (13.6 ind ha−1) adjacent to the mouths of the Grijalva-Usumacinta and San Pedro–San Pablo rivers (18°55´N, 92°42´W. 33.8 m depth) and during day in 2013 (13.2 ind ha−1), in the vicin- ity of Carmen Inlet (18°44´N, 91°54´W, 6.1 m depth) (Fig. 1C, D). For each stomato- pod species, the two-way ANOVA test (Table 2) indicated that the mean densities 184 Bulletin of Marine Science. Vol 92, No 2. 2016
Table 1. Summary statistics for stomatopod density in Campeche Sound during the 2012 and 2013 rainy seasons.
Squilla chydaea Squilla empusa Density (ind ha−1) Density (ind ha−1) Sampling Number Total Total Year time of trawls abundance Mean (SE) Min–max abundance Mean (SE) Min–max 2012 Day 22 49 0.89 (0.45) 0–8.4 12 0.22 (0.12) 0–2.4 Night 4 25 2.50 (1.56) 0–6.8 47 4.70 (3.08) 0–13.6 2013 Day 23 6 0.10 (0.08) 0–1.6 59 1.03 (0.61) 0–13.2 Night 11 26 0.95 (0.37) 0–4.0 10 0.36 (0.19) 0–2.0 Overall Day 45 55 0.49 (0.23) 0–8.4 71 0.63 (0.32) 0–13.2 Night 15 51 1.36 (0.50) 0–6.8 57 1.52 (0.91) 0–13.6 Pooled 60 106 0.71 (0.21) 0–8.4 128 0.85 (0.33) 0–13.6 varied significantly with year (2012 > 2013; P < 0.1, after Bonferroni correction) and sampling time (night > day; P < 0.1, after Bonferroni correction). For S. empusa, the year × sampling time interaction term was significant (night 2012 > day 2012 = night 2013 = day 2013; P < 0.1, after Bonferroni correction). The highest mean density was observed for S. empusa during night sampling in 2012, which was 47-times higher than the lowest density of S. chydaea, sampled during the day in 2013 (Table 1). In both years, t-tests indicated that the mean depths inhabited by S. chydaea and S. empusa were significantly different. In 2012, the mean sampled depth of S. chydaea was 53.7 m (SE 5.2, range: 40.0–81.9 m), and the mean sampled depth for S. empusa was 31.9 m (SE 3.4, range: 19.0–43.6 m) (t-test = 3.399, P = 0.0039). In
Figure 1. Population density distribution of the stomatopods (A–B) Squilla chydaea and (C–D) Squilla empusa during the 2012 and 2013 rainy seasons in Campeche Sound. May-Kú et al.: Squilla stomatopods in Campeche Sound 185
Table 2. Results of two-way analysis of variance testing stomatopod species density (ind ha−1) between years (2012, 2013) and sampling times (day, night). Density data were transformed by log (x+1). MS = the mean sum of squares. * = significant probability atP < 0.1.
Source of variation df MS F P Squilla chydaea Year 1 0.201 3.705 0.0593* Sampling time 1 0.485 8.923 0.0042* Year × sampling time 1 0.009 0.170 0.6816 Error 56 0.054 Squilla empusa Year 1 0.309 5.129 0.0274* Sampling time 1 0.469 7.796 0.0072* Year × sampling time 1 0.659 10.949 0.0016* Error 56 0.060
2013, corresponding depths were 67.9 m (SE 10.9, range: 35.0–131 m) and 22.6 (SE 4.3, range: 6.1–42.0 m) (t-test = 3.989, P = 0.0009) for S. chydaea and S. empusa, respectively. For S. chydaea, the NB2 model (quadratic) fit the density vs water depth data much better than the other models tested (2012: NB2 = 67.3 AIC, NB1 = 72.2 AIC, Poisson = not adjusted; 2013: NB2 = 49.7 AIC, NB1 = 54.9 AIC, Poisson = not adjusted). The quadratic model accounted for 35.6% of the total variance in 2012 (F1,23 = 7.83, P =
0.005) and 39.2% in 2013 (F1,31 = 13.89, P = 0.0001). Considering both years, the high- est expected densities of S. chydaea are found in the depth range from 60 to 120 m. It is expected that outside this range their densities will decrease sharply, reaching 0 ind ha−1 at depths below 30 m and above 160 m (Fig. 2C, D). For S. empusa, the NB1 model (linear) fit the density vs water depth data much better than the other models tested (2012: NB1 = 54.2 AIC, NB2 = 60.0 AIC, Poisson = not adjusted; 2013: NB1 = 68.1 AIC, NB2 = 69.9 AIC, Poisson = not adjusted). The linear model accounted for
17.5% of the total variance in 2012 (F1,24 = 3.68, P = 0.054) and 41.3% in 2013 (F1,32 = 8.71, P = 0.003). Pooling years, densities of S. empusa decrease as water depth in- creases, with the highest densities at <30 m depth and reaching 0 ind ha−1 at >50 m (Fig. 2C, D).
Discussion
The stomatopods collected in the present study included two of the five sympatric Squilla species reported in Campeche Sound: S. chydaea and S. empusa (Reaka et al. 2009). This species composition is similar to that found by Ruiz (2008) and Ruiz et al. (2013), who indicated that both stomatopod species contribute about 30%–40% to the total abundance of the epibenthic macro-crustacean fauna of Campeche Sound. Squilla e. edentata is mainly a deep-water species (found from 148 to 369 m; Reaka et al. 2009), which may explain its absence at our sampling sites. Squilla deceptrix and S. rugosa are not abundant in Campeche Sound and have been reported in habi- tats that were not included in the present study, such as coral reefs and rocky or 186 Bulletin of Marine Science. Vol 92, No 2. 2016
Figure 2. (A–B) Distribution of relative abundance with water depth for the stomatopods Squilla chydaea and Squilla empusa. (C–D) Negative binomial generalized linear models fitted for popu- lation density of S. chydaea (black line) and S. empusa (gray line) by water depth. Dashed lines represent the 95% confidence interval. shell-dominated substrates (Reaka and Manning 1987, Vázquez-Bader and Gracia 1994, Arenas-Fuentes and Hernández-Aguilera 2000). In the present study, mean densities of S. chydaea and S. empusa tended to be great- er at night than during the day. To our knowledge, there is no published information comparing densities of S. chydaea during day and night. For S. empusa, Rockett et al. (1984) caught significantly more individuals in night trawls in the northwestern Gulf of Mexico. However, S. empusa is both diurnally and nocturnally active (Cronin 1992) and has been caught in large numbers during the day (Wenner and Wenner 1988) as well as at night (Wortham 2009, Syuhada 2011). Their nocturnal abundances can be negligible in some seasons (Manning and Heard 1997). Most stomatopod studies characterize the diversity of species based on total or relative abundance (e.g., Hendrickx 1984, Barbosa-Ledesma et al. 2000, Hendrickx and Sánchez-Vargas 2005, Araújo et al. 2013). Very few studies have reported the population density (number of individuals per unit area) for multiple Squilla species, which is useful for inter-study comparisons. The densities we observed are similar to those reported for S. mantis in the Mediterranean Sea (mean density of 1.72 ind ha−1, minimum of 0.2 ind ha−1, and maximum of 8.85 ind ha−1), where this species is tradi- tionally caught only during daylight hours (Ragonese et al. 2012). However, across all times of day, the mean densities of S. chydaea (0.71 ind ha−1) and S. empusa (0.85 ind ha−1) observed in the present study are 35- to 94-times lower than the mean densities reported for these species in Campeche Sound during the 1994–1995 rainy seasons (24.8 and 80.3 ind ha−1, Ruiz 2008). Considering only the mean maximum values May-Kú et al.: Squilla stomatopods in Campeche Sound 187 we obtained at night 2012, the densities of S. chydaea (2.5 ind ha−1) and S. empusa (4.7 ind ha−1) are 10- to 17-times lower than the mean density observed during the 1994–1995 rainy seasons (Ruiz 2008). Our mean densities are also much lower than night collections of S. empusa in Narragansett Bay, Rhode Island, USA. This species is commercially fished in the bay, where mean densities of 0.02 ind −2m (200 ind ha−1) and 1.7 ind m−2 (17,000 ind ha−1) have been reported using otter trawls and under- water video observations, respectively (Syuhada 2011). In addition, the mean densi- ties recorded at night for Squilla hancocki Schmitt, 1940 (44 ind ha−1) and Squilla panamensis Bigelow, 1891 (58 ind ha−1) on the continental shelf of Jalisco and Colima (Mexico) are much higher than our densities (Arciniega-Flores et al. 1998). It is possible that we underestimated the stomatopod densities by sampling with an otter trawl. However, in Campeche Sound, catches of other crustaceans, such as penaeid shrimps, have also declined drastically in the last 40–50 yrs, decreasing from >15,000 t yr−1 in the 1960–1970s to approximately 2000 t yr−1 during the period from 2004 to 2013 (SAGARPA 2013). It has been suggested that excessive fishing ef- fort, over-exploitation of juvenile stages, and increased oil production in the area are the main factors leading to declines in penaeid shrimp production (Soto et al. 2014); but it is unknown if other benthic crustaceans, such as stomatopods, are also experi- encing population declines. Further studies, preferably over longer time periods (e.g., including dry and cold front months not included in the present study), are necessary to understand whether the apparent decline in population density of S. chydaea and S. empusa in Campeche Sound is due to natural temporal fluctuations or anthropo- genic disturbances. In the present study, S. chydaea was collected at higher densities in deeper water compared to S. empusa. Depth segregation between these stomatopod species has also been observed in other sectors of the Gulf of Mexico, with S. chydaea distrib- uted in deeper offshore waters andS . empusa in nearshore shallow waters (Rockett et al. 1984, Wenner and Wenner 1988, Wortham 2009). Depth segregation is common in sympatric stomatopod species off Brazil (Araújo et al. 2013), in the Mediterranean Sea (Abelló et al. 1993–1994), and in the Gulf of Tehuantepec (Mexico; Barbosa- Ledesma et al. 2000). Several biotic and abiotic factors may explain these inter-spe- cific differences in depth distribution, including intra- and interspecific agonistic and competitive interactions that allow the efficient utilization of common resources such as space and food (Caldwell and Dingle 1975), segregation of populations into different habitats (or sediment types) to reduce predation risk (e.g., Hernáez et al. 2011, Araújo et al. 2013), and inter-specific differences in physiological ability to cope with salinity and temperature gradients (Morgan 1980, Wortham 2009). In the pres- ent study, relatively high densities of S. empusa were observed near river mouths, where low salinities and muddy sediments prevail (Hernández-Arana et al. 2005). In the northern Gulf of Mexico, salinity and temperature gradients influence abun- dance and distribution of both stomatopod species; S. empusa is collected in warmer and lower salinity waters than S. chydaea (Wortham 2009). High abundances of S. empusa on muddy sediments have also been observed in Campeche Sound (Vázquez- Bader and Gracia 1994, Ruiz et al. 2013), the northern Gulf of Mexico (Rockett et al. 1984), the North Atlantic (Syuhada 2011), and the South Atlantic (Araújo et al. 2013). In the Mediterranean Sea, the commercially targeted species S. mantis inhabits shal- low waters (10–50 m in depth) in the vicinity of river mouths that are character- ized by muddy sediments (Ragonese et al. 2012). On the other hand, S. chydaea has 188 Bulletin of Marine Science. Vol 92, No 2. 2016 been collected on different sediment types, such as silty-clay, silty-sand, and mud (Vázquez-Bader and Gracia 1994, Ruiz et al. 2013). In our study, S. chydaea was mainly caught offshore off Terminos Lagoon, which, according to Hernández-Arana et al. (2005), is an area characterized by calcareous sediments, ranging from very coarse to medium-silt, mixed with terrigenous material (carbonate content >50%). Given the important ecological role of stomatopods, as well as their potential for commercial harvest and use as environmental indicators, knowledge of their spatial and temporal patterns in distribution and abundance may be useful information for the management of these species. Variable densities across day and night, and across different depths in the southern Gulf of Mexico, indicate that these species can vary widely in their abundance patterns. Apparently, lower densities of S. chydaea and S. empusa observed over the past 20 yrs highlight the need for long-term data sets of population density to monitor trends across the seasons and years.
Acknowledgments
Data used in this study are part of the southern Gulf of Mexico Environmental Monitoring Program carried out by PEMEX Exploración y Producción (Regiones Marinas) and Cinvestav- Mérida. The authors are grateful to Julio Duarte-Gutierrez for his help with species identifica- tion and Orlando Lam-Gordillo (Benthos Laboratory, Cinvestav) for his assistance with GLM analysis. Thanks are also due to K Grorud-Colvert for her help with English editing. We thank SAGARPA for permit DGOPA.13993.111012.3263 to collect biological material for scientific purposes.
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