Seasonal vertical distribution of fish larvae in the southern Gulf of Mexico

Distribución vertical estacional de larvas de peces en el sur del Golfo de México

María de la Luz Espinosa-Fuentes,¹ César Flores-Coto,¹ Faustino Zavala-García,¹ Laura Sanvicente-Añorve¹ and René Funes-Rodríguez²

¹ Laboratorio de Zooplancton, Instituto de Ciencias del Mar y Limnología, Universidad Nacional Autónoma de México. AP 70-305, México DF, 04510. México.

Recibido: 23 de enero de 2012.
Aceptado: 2 de enero de 2013.

ABSTRACT

Changes in the composition and abundance of fish larvae in the water column were analyzed throughout an annual cycle (1994-1995) in the southern Gulf of Mexico, in order to establish the difference between the habitat of the larvae and the effect of oceanographic events on larval vertical distribution. The study area comprised the continental shelf off Tabasco and Campeche in the southern Gulf of Mexico. Samples were collected at five water column levels: 0-6, 6-12, 12-18, 45-55 and 95-105 m. A total of 118 taxa were identified, 52 were dominant species, 33 were larvae of neritic parents and 19 were larvae of mesopelagic parents. The results indicate that the water column presented two layers above the 105 m depth: a surface layer (0-18 m) and a deep layer (45-105 m). The greatest density of larval species that inhabit neritic areas as adults was recorded in the surface layer (0-18 m), while larvae of which the parents inhabit mesopelagic areas were found in the deep layer (45-105 m). The mixing of the water column was the most important physical factor regarding the variation in the vertical distribution of the larvae of both groups, particularly in winter. However, the biology of each species and the habit to occupy a particular depth was the most important factor that determined their distribution in the water column.

Key words: Larval fish, mixing processes, neritic habitat and mesopelagic habitat, vertical distribution.

RESUMEN

Palabras clave: Distribución vertical, hábitat nerítico, hábitat mesopelágico, larvas de peces, procesos de mezcla.

INTRODUCTION

Studies on ichthyoplankton have become important since the beginning of last century in view of its close relationship with fisheries. Studies on the early life history of fish have been useful in developing a better understanding of fish population dynamics and determining the causes of major fluctuations in fish stock production (Blaxter, 1974; Smith, 1981; Trippel & Chambers, 1997; Fuiman, 2002).

Studies on larval fish communities necessarily require an analysis of hydrological processes such as currents, eddies and upwellings (John, 1985; Röpke, 1993; Rodríguez et al., 2006; Sánchez-Velasco et al., 2007; Aceves-Medina et al., 2008), particularly in the case of neritic areas that receive freshwater discharges and present river fronts, mixing processes and stratification (Gray, 1996; Reiss & McConaugha, 1999).

These studies generally include meso-scale processes. However, in order to obtain a better understanding of the conformation and variations in the communities, a fine-scale study of dozens of meters along the vertical distribution is required (Espinosa-Fuentes & Flores-Coto, 2004; Okazaki & Nakata, 2007; Sánchez-Velasco et al., 2009; Hsieh et al., 2010).

Previous studies on the vertical distribution of fish larvae in several regions of the world have recorded different groups of species with different distribution patterns. Similarly, larvae of shelf dwelling species generally occur in the surface layer of the ocean, while those of mesopelagic species live in the deeper layers (Loeb, 1979; Röpke, 1993; Cha et al., 1994; Conway et al., 1997; Gray & Kingsford, 2003; Sabatés, 2004).

Species distribution patterns are the result of an evolutionary adjustment of larval habits to the hydrographic processes that guarantee their survival. However, no studies on the yearly seasonal variations of these patterns have been carried out, and it is assumed that they differ according to the geographical area, particularly where strong discharges of freshwater are received.

The southern Gulf of Mexico is a very dynamic area with currents, eddies and wind effects, and continental shelf waters that receive a strong fluvio-lagoon influence. The main freshwater discharge in this area is provided by the Grijalva-Usumacinta river system that generates haline fronts and low salinity and low temperature areas, mostly at surface (~15 m). The greatest salinity variations occur during the rainy months, from June to October (Czitrom et al., 1986; Monreal-Gómez et al., 1992), when the water column is stratified by a thermocline at a depth of 20 to 30 m. Lower temperatures and a deeper mixing layer (70-100 m) have been recorded during the winter, when the presence of cold fronts known as "northers" is common (Alatorre et al., 1989).

MATERIALS AND METHODS

The study area spans the continental shelf of the southern Gulf of Mexico (18º-20º N, 91º-94º W) (Fig. 1). Twenty two sampling stations distributed along four transects, perpendicular to the coastline, were established off the states of Campeche and Tabasco (Fig. 1). Sampling was carried out in May 21-30 (spring), August 19-29 (summer) and November 17-27 (autumn) of 1994 and in February 7-17 (winter) of 1995.

Samples were collected with a multiple open-closure net plankton system with a 75 cm diameter, a 500 µm mesh size and General Oceanic flowmeters, at five levels in the water column: level 1 (0-6 m), level 2 (6-12 m), level 3 (12-18 m), level 4 (45-55 m) and level 5 (95105 m). Samples were preserved with 4% formalin neutralized with sodium borate. Larval fish were sorted and identified to the lowest taxonomic level possible according to Richards (2006). The specimens identified to the level of species were included in the seasonal variation analysis. Larvae density (LD) was standardized at 100 m³:

Since the spatial distribution of plankton is not homogeneous, the geometric mean (GM) was calculated from the density of larvae at each sampling level (Zar, 2010).

The Importance Value Index (IVI) was applied in order to define the most important species for each level and season, considering the total percentage of abundance (% A) and the frequency of occurrence (% F). Only the species that reached an IVI value greater than 5% were analyzed. The analysis was carried out using the ANACOM software (De la Cruz-Agüero, 1994).

The continental shelf was divided into inner, middle and outer based on the location and depth of the sampling stations in order to analyze the horizontal distribution of the larvae (Table 1).

An Analysis of Variance (ANOVA) was applied at a significance level of 0.05 for each sampling period in order to identify significant differences on the continental shelf related to the distribution of fish larvae density. A Tukey test was used for post hoc comparisons (Zar, 2010).

Salinity and temperature data were obtained with a Neil Mark IV CTD at each sampling period. The degree of stratification of the water column was estimated calculating the potential energy anomaly or φ parameter (Simpson et al., 1978).

The influence of the physical parameters, temperature, salinity and potential energy anomaly (stratification or mixing of the water column) on the vertical distribution of fish larvae was established by the Canonical Correspondence Analysis (CCA) using the ANACOM software (De la Cruz-Agüero, 1994).

RESULTS

Water temperature was homogeneous during May, August and November 1994, with a mean of 28 °C from the surface to a depth of 18 m (levels 1, 2 and 3) and 20 °C to 24 °C in the deeper levels (45 and 105 m). In February 1995, the mean temperature was 24 °C from the surface down to 70 m and 18.8 °C at 100 m (Fig. 2).

Salinity at the surface layer (0-18 m) varied from 36.2 to 37.4 in May. It decreased greatly during the rainy season (August to November) with the lowest value of 34.0 near the shore and the highest of 36.4 in offshore waters. In February, salinity and temperature presented a similar vertical distribution with homogeneous values from the surface to 70 m, as well as a coast-ocean gradient with values of 35.2 to 36.8 (Fig. 3).

The mixing layer was present from the surface to a depth of 30 m with φ values <40 J m^-3 during May, August and November. In deeper waters (100 m), the φ increased to more than 250 J m^-3 indicating a marked stratification. In February, the mixing layer reached 70 m with a φ <50 J m^-3 and at 100 m the φ was ~150 J m^-3 (Fig. 4).

A total of 63,655 specimens of 118 taxa of larval fish were identified (Table 2) for the four seasons and five sampling levels in the water column (depths of 0 to 105 m). There were 52 dominant species according to the IVI, 33 were species of neritic parents and 19 were mesopelagic dwellers. Among the dominant species, only nine were observed in all the periods: Auxis rochei Risso, 1810, Benthosema suborbitale Gilbert, 1913, Bothus ocellatus Agassiz, 1831, Bregmaceros cantori Milliken & Houde, 1984, Cynoscion arenarius Ginsburg, 1930, Hygophum taaningi Becker, 1965, Selar crumenophthalmus Bloch, 1793, Syacium gunteri Ginsburg, 1933 and Syacium papillosum Linnaeus, 1758.

The distribution across the continental shelf of larvae of neritic fish presented a coast-ocean gradient in all the sampling periods, with the greatest density values on the inner and middle shelves (>62%) and significantly lower values towards the outer shelf (<38%) (Table 3).

This distribution pattern was confirmed through the ANOVA and Tukey multiple range tests which indicated significant differences (p < 0.05) between the larval density of the inner and middle shelves, and that of the outer shelf.

The greatest average density on the inner and middle shelves was recorded at level 2 (6-12 m) with species of the Carangidae and Sciaenidae families as the most representative (Table 4, Table 5, Table 6, Table 7).

As the results indicated that the larval distribution of the neritic and mesopelagic species was not homogeneous across the continental shelf, the analysis of the vertical larval distribution was carried out exclusively for the outer shelf stations where specimens were collected from the five sampling levels.

The Bray-Curtis dissimilarity index clearly defined two groups of fish larvae in the water column of these stations. During spring, summer and autumn, the first group was formed by larvae located at the surface (0 to18 m, levels 1, 2 and 3) and the second group consisted of larvae of the deeper layer (45 and 105 m, levels 4 and 5) (Figs. 5A-C). During the winter, the first group was formed by larvae of levels 1, 2, 3 and 4 (0-45 m) and the second group had the larvae of level 5 (105 m) (Fig. 5D).

The results indicate that there were two layers in the first 105 m of the water column: a surface and a deep layer.

Larvae of neritic fish presented their greatest abundance in the surface layer (> 85%) at all times, whereas the larvae of mesopelagic parents recorded more than 74% of their total density in the deep layer, except for winter when they represented only 64% (Table 8). The high percentages of neritic and mesopelagic components in the surface and deep layers respectively show that the larvae remain in a particular stratum all the time.

In the spring, 47 species were dominant (IVI > 5%), 31 were neritic and 16 were mesopelagic. Six neritic species, Chloroscombrus chrysurus Linnaeus, 1766, Euthynnus alletteratus Rafinesque, 1810, Scomberomorus cavalla Cuvier, 1829, Sphyraena guachancho Cuvier, 1829, Trachurus lathami Nichols, 1920 and Trichiurus lepturus Linnaeus, 1758 occurred exclusively in the surface layer, while the species Balistes capriscus Gmelin, 1789, Bothus ocellatus, Lutjanus campechanus Poey, 1860, Selene setapinnis Mitchill, 1815 and Syacium papillosum occurred throughout the water column (Table 4).

In the deep layer, the most abundant mesopelagic species, including Benthosema suborbitale, Hygophum taaningi and Myctophum asperum Richardson 1845, were recorded exclusively in this depth layer (Table 4, Fig. 6A).

In the summer, the IVI recorded 43 dominant species, 29 in the surface layer and 14 in the deep layer. The most abundant species in the surface layer were Pristipomoides aquilonaris Goode & Bean 1896, Scomberomorus cavalla and Sphyraena guachancho. The larvae of mesopelagic fish were all restricted to the deep layers, with the most representative being Lobianchia gemellarii Cocco, 1838, Hygophum macrochir Günther, 1864 and Myctophum nitidulum Garman, 1899 (Table 5, Fig. 6B). The presence in this depth layer of Bregmaceros cantori, with 96% of its abundance, must be mentioned. Species including Syacium gunteri, Bothus ocellatus and Selene setapinnis were found throughout the water column (Fig. 6B).

In the winter, the IVI identified 41 dominant species of which 27 were neritic and 14 were mesopelagic. The larval distribution throughout the water column presented a mixture of neritic and mesopelagic species, with these last recording a density of 35% at the surface layer (Table 8).

Hygophum macrochir, Lestidiops jayakari Boulenger, 1889, Myctophum nitidulum Garman, 1899 and Notolychnus valdiviae Brauer, 1904, which at other times have shown a greater affinity for deeper waters, were observed in the surface layer, with some even reaching level 1. Furthermore, neritic species like Chloroscombrus chrysurus, Auxis rochei, Stellifer lanceolatus, Trachurus lathami and Trichiurus lepturus which had occupied the surface levels (6-45 m) in the previous months, were observed in the deeper waters (level 5) (Table 7, Fig. 6D).

Neritic species like Auxis rochei, Bothus ocellatus, Cyclopsetta fimbriata Goode & Bean, 1885, Selene setapinnis, Selar crumenophthalmus, Sphyraena guachancho, Syacium gunteri and Syacium papillosum presented a wide distribution throughout the water column in all the sampling periods, though their greatest abundance was recorded in the surface layers. Other species also occurred in all the depth levels, but not in all the seasons (Tables 4, Table 5, Table 6, Table 7).

With respect to the larvae of mesopelagic species, Diogenichthys atlanticus Tåning, 1928, Hygophum hygomii Lütken, 1892, Hygophum taaningi, Myctophum nitidulum, Vinciguerria poweriae Chevrolat, 1863 and Maurolicus muelleri Gmelin, 1789 were present in different seasons always in the deep layer (Table 4, Table 5, Table 6, Table 7).

The CCA applied to the data recorded in May yielded a species-environment correlation of 0.99 for the first axis, of 1.00 for the second axis and of 0.96 for the third axis. The potential energy generated the greatest variability in axes I and II. Neritic species like Auxis rochei, Caranx crysos Mitchill, 1815, Balistes capriscus and Microdesmus bahianus Dawson, 1973 presented a direct relationship with temperature and salinity, whereas mesopelagic species like Bregmaceros cantori, Benthosema suborbitale and Notolychnus valdiviae, among others, did so with the potential energy anomaly (Fig. 7A).

In August, the species-environment correlations were 1.0, 0.99 and 0.83 in axes I, II and III respectively. The species Bothus ocellatus, Syacium gunteri and Balistes capriscus were directly related to salinity and temperature, whereas the mesopelagic species were related more with the potential energy anomaly (Fig. 7B).

The CCA in November presented a species-environment correlation of 0.99 for axes I and II, and of 0.62 for the third axis. The neritic species were mostly related to the temperature and salinity, particularly the larvae of the families Carangidae, Sciaenidae and the flatfish. The larvae of the mesopelagic Ceratoscopelus warmingii Lütken, 1892, presented a direct relationship with salinity in this season, while the neritic Bregmaceros cantori did so with the potential energy anomaly (Fig. 7C).

The CCA for February 1995 revealed a species-environment correlation of 0.99 for the first axis, of 0.84 for the second and of 0.96 for the third. Temperature and salinity presented a strong positive relationship with both neritic and mesopelagic species like Cynoscion arenarius, Bothus ocellatus, Trichiurus lepturus, Lestidiops jayakari and Hygophum macrochir. Species that were generally located in the deeper layer, including Notolychnus valdiviae, Benthosema suborbitale and Hygophum higomii, presented a direct relationship with the potential energy anomaly (Fig. 7D).

The results obtained clearly indicate that fish larvae present a cross-shelf distribution that is directly related to the habitat of the adults. The larval composition on the inner shelf consisted mainly of species of which the adults are estuarine-dependent or are linked to coastal areas that receive a fluvio-lagoon influence, while the larvae of mesopelagic adult fish presented their greatest densities in the oceanic areas. An inshore-offshore gradient of fish larvae has been reported for other places (Leis, 1982; Smith et al., 1999; Gray & Miskiewicz, 2000; Catalán et al., 2006; Alemany et al., 2006, 2010).

The results also showed that the larvae of species that inhabit neritic waters as adults presented their greatest diversity and density at the surface layer (0-18 m), whereas the larvae of species that inhabit oceanic areas as adults occupied the deeper waters (45-105 m), with only a few species occasionally occupying the surface layer. Similar results have been observed in the Mediterranean Sea (Sabatés, 2004), the southeastern coast of Australia (Gray, 1993; Gray & Kingsford, 2003) and the western tropical Atlantic (Cha et al., 1994). The larvae of Bregmaceros cantori, a neritic species (Zavala-García & Flores-Coto, 1994), broke the distribution pattern of the neritic species, when its greater abundance was recorded in the deep layer, except for winter when it occurred at all depths.

Differences were observed in the vertical distribution of the larvae of some groups of species. The larvae of the Carangidae, Sciaenidae and Scombridae mainly occupied the surface layer and were very scarce in deeper layers, coinciding with other records on the distribution of these families (Boehlert & Mundy, 1994; Flores-Coto et al., 1999, 2001; Comyns & Lyczkowski-Shultz, 2004; Torres et al., 2011).

On the other hand, Pleuronectiformes larvae, including those of the Bothidae, Paralichthydae and Cynoglosidae, presented a wide distribution throughout the water column, with relatively high densities in the deep layers.

The deep levels (45-105 m) were characterized by the presence of fish larvae of oceanic dwellers, including Bregmaceros atlanticus and members of the families Myctophidae, Gonostomatidae and Phosichthyids (Flores-Coto & Ordoñez-López, 1991; Zavala-Garcia & Flores-Coto, 1994; Gôngora-Goçalo et al., 2011).

The recorded distribution patterns reflect the behavior and preference of each species to maintain a certain position in the water column. According to Olla and Davis (1990), fish larvae possess behavior mechanisms that enable them to alter their position in the water column to deal with environmental gradients and select favorable ones. On the other hand, the preference of a certain depth stratum has been associated with biological and environmental stimuli that ensure the best larval survival (Boehlert & Mundy, 1988; Heath, 1992; Cha et al., 1994; Olivar & Sabatés, 1997; Aceves-Medina et al., 2008).

During spring, summer and autumn, the vertical distribution pattern of larvae on the outer shelf indicated the presence of two groups of species in the water column, a neritic group that mostly occupied the surface layer (0-18 m) and a mesopelagic group confined to the deeper layer (45-105 m). Apart from the larval habit to remain in a particular layer, distribution patterns may be related to the water column hydrodynamics. During the seasons of this study, the neritic organisms were generally confined to the mixing surface layer at ~30 m.

The CCA corroborated a direct relationship between the neritic species and high values of salinity and temperature, mainly in the upper layers, as has been reported by Tzeng and Wang (1993) and Miranda et al. (2006), while mesopelagic larvae presented a greater affinity with high values of stratification.

The presence of the same two groups of species was observed in winter as well. However, the vertical distribution of some mesopelagic species was not confined to the deep layer. Larvae of several species were distributed more widely in the water column. This may be related to the depth of the mixing layer which at this time of the year reached 70 m and favored the mixing of surface and deep species. This was confirmed by the CCA data for this season.

Such changes in the distribution of species during mixing processes have been documented by various authors for other regions, and it has been concluded that vertical mixing may modify patterns of vertical distribution of planktonic organisms (Incze et al., 1990; Haury et al., 1990; Legadeuc et al., 1997; Farstey et al., 2002).

The results make it possible to observe a strong contrast between the high larval density at the surface, mainly of neritic species, and the low larval densities in the deep layer that correspond to the mesopelagic species for the four seasons. The greatest difference between the surface and the deep layers was observed in the spring and the smallest in the winter, probably because at that time a greater number of larvae of mesopelagic species ascended from deeper levels that were not sampled.

The greater concentration of larvae in the surface layer of the oceans, generally above 50 m, has been linked to food availability (Röpke, 1993; Conway et al., 1997; Gray, 1998; Sabatés, 2004; Sánchez-Velasco et al., 2009). Rodríguez et al. (2006) also mentioned that there is a trophic relationship between fish larvae and mesozooplankton, and consequently the distribution of prey may play an important role in the vertical distribution of larvae.

The study area that includes the first 105 m of the water column is characterized by the presence of two major layers, a surface layer (0 to 18 m) with a greater abundance of neritic species and a deeper layer (45 to 105 m) with more species that have an affinity for oceanic environments.

The mixing process in the water column was the most important physical factor to affect the vertical distribution of larvae, particularly in winter. However, regarding the habits of the larvae of each species, the preference to stay of a certain depth was the most important biological factor that determined their distribution in the water column.

ACKNOWLEDGEMENTS

The authors express their gratitude to Dr. J. Kasper-Zubillaga and Dr. Oscar Peralta for their valuable assistance, and DGAPA-UNAM for its financial support (grants IN-202092 and IN-203893). They also thank the three reviewers for their comments and interest in this paper.

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