Journal of Sea Research 59 (2008) 173–185 www.elsevier.com/locate/seares

Ecological and biological strategies of Etropus crossotus and Citharichthys spilopterus (Pleuronectiformes:) related to the estuarine plume, Southern Gulf of Mexico ☆ ⁎ Patricia Sánchez-Gil a, , Alejandro Yáñez-Arancibia b, Margarito Tapia a, John W. Day c, Charles A. Wilson c, James H. Cowan Jr. c

a Universidad Autónoma Metropolitana Iztapalapa, Departamento de Hidrobiología, Ap. Post. 55-535, México D.F. b Unidad Ecosistemas Costeros, Instituto de Ecología A.C. Km 2.5 Antigua carretera a Coatepec # 351, El Haya 91070, Xalapa Ver., México c Louisiana State University, Department of Oceanography and Coastal Sciences, Baton Rouge, LA 70803, USA Received 25 September 2007; received in revised form 3 December 2007; accepted 4 December 2007 Available online 23 December 2007

Abstract

Differences in the biological and ecological strategies of two tropical , Etropus crossotus (fringed ) and Citharichthys spilopterus () are discussed. The comparative analysis was based on the seasonal distribution of relative abundance of the two species and movements utilizing estuarine plume influenced areas as part of their life cycles. Growth parameters of the von Bertalanffy equation and recruitment were estimated (FISAT software) to compare life cycle patterns. The recruitment patterns illustrate the key difference between “estuarine-dependent” and “estuarine-related” nekton strategies. Both species have a short life cycle with a continuous recruitment activity. E. crossotus is an estuarine-related species, with two recruitment pulses (winter frontal season), in the estuarine plume on the shelf. C. spilopterus is an estuarine-dependent species, with a main recruitment pulse during the rainy season in the estuarine plume, and a residual secondary pulse inside the adjacent estuarine system (Terminos Lagoon). The results show that the ecological success of these tropical coastal marine flatfish, with similar biological patterns, is based upon the sequential use (in time and space) of estuarine plume influenced habitats, suggesting that fish migration to shallow waters is related to food availability changes as a strategy towards optimum recruitment. © 2007 Elsevier B.V. All rights reserved.

Keywords: Flatfish ecology; Tropical recruitment; Estuarine dependence; Estuarine plume; Gulf of Mexico

1. Introduction

In the southern Gulf of Mexico, the three main species ☆ This article is part of the PhD dissertation of the senior author, of flatfishes, in order of abundance, are Syacium gunteri, Doctorado en Ciencias Biológicas, Universidad Autónoma Metropo- Citharichthys spilopterus and Etropus crossotus. Sánchez- litana. Iztapalapa, México D.F. Gil and Yáñez-Arancibia (1986) presented a detailed ⁎ Corresponding author. description of the distribution and abundance of these E-mail addresses: [email protected] (P. Sánchez-Gil), [email protected] (A. Yáñez-Arancibia), species and determined that these three species are [email protected] (M. Tapia), [email protected] (J.W. Day), ecologically important in the structure and function of the [email protected] (C.A. Wilson), [email protected] (J.H. Cowan). demersal fish community. The ecological dominance of

1385-1101/$ - see front matter © 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2007.12.002 174 P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185 demersal fish species in tropical coastal areas can be conditions in the tropical estuarine plume on the inner determined by their high frequency, high relative abun- shelf of the southern Gulf of Mexico. Specific objectives dance and high density (Sánchez-Gil et al., 1981). This are: to determine spatial distribution patterns of E. dominance results from the ability of these species to crossotus and C. spilopterus, to document seasonal compete in intricate food webs comprised of species that fill changes in terms of relative abundance, to establish similar niches (Pauly, 1982). In Campeche Sound, Syacium what characteristics determine differences in their life gunteri represented 3 to 17% of wet weight in experimental history patterns, and which strategies permit them to co- catch trawls, Etropus crossotus from 0.1 to 2.8% and exist as dominant species in a high diversity context. We Citharichthys spilopterus from0.2to1.2%(Sánchez-Gil hypothesized that these dominant species use the shelf- and Yáñez-Arancibia, 1986). The study of dominant estuarine-lagoon environment in different spatial and flatfish species allows an understanding of their function temporal patterns as a strategy to reduce the effects of in the fish community and the specific strategies that they competition and predation, and to increase the likelihood have evolved to successfully coexist. Froese and Pauly of recruitment success. In both cases, the sequential use of (1994) reported that there is relatively little information the area is closely tied to the estuarine plume. about several life history parameters in flatfishes such as: a) degree of concentration in nursery areas compared to adult 2. Area description distribution; b) age at metamorphosis; c) the seasonal peak of female fecundity parameters and; d) natural mortality 2.1. Habitat characterization estimates of eggs and 0-groups. In particular, there is limited information on flatfishes from tropical zones with A) Habitat characteristics and environmental variabil- regard to: 1) the separation of life history in different coastal ity in Campeche Sound in the southern Gulf of habitats; 2) the seasonal variation of abundance; and, 3) Mexico (Fig. 1) were described in detail by Yáñez- recruitment strategies. These issues are especially difficult Arancibia and Sánchez-Gil (1986).Theydeter- in tropical areas where hundreds of similar species co- mined that the main environmental characteristics occur, and attribution of eggs to their respective species is of the study area are: A) The presence of three difficult, if not impossible. This consideration concerning climatic seasons; 1) a dry season from February to eggs in many cases also applies to larvae because the rapid May; 2) a rainy season from June to September; development time of larval stages. This implies that and, 3) the “nortes” or winter storms season from methodologies for the quantitative study of recruitment in October to February. This climatic sequence tropical demersal communities can begin with early controls different seasonal pulses in ecosystem juveniles at best (Yáñez-Arancibia and Pauly, 1986; dynamics, including temperature gradients, estuar- Pauly, 1994). ine and riverine discharge to the shelf, and detrital Reflecting these concerns, ten years ago, García-Abad biomass in estuarine plume influenced areas on the et al. (1992) and Sánchez-Gil et al. (1994) proposed a shelf (Sánchez-Gil et al., 1994)(Fig. 2). conceptual model of recruitment for Syacium gunteri in B) Terminos Lagoon is a representative estuarine the southern Gulf of Mexico relating recruitment strategies ecosystem in the southern Gulf of Mexico, with to the dynamics of primary productivity in the ecosystem. precipitation ranging from 1700 to 2000 mm/year, These papers represented a significant advance of knowl- (Yáñez-Arancibia et al., 2004), aquatic primary edge of the biology, ecology, early life history and hence productivity of 333 mg Cm3/hr (Day et al., 1988), recruitment studies based on early juvenile parameters of and 214 fish species (Lara-Domínguez et al., one of the most important flatfish in the Mexican tropical 1993). The lagoon has a moderate seasonal pulse coastal zone. of temperature and light, and a strong semi- In a similar context, this paper shows the interactions permanent physical-chemical gradient from the that occur within the estuary and adjacent sea shelf, areas sea to the river mouths, as well as a high diversity that exhibit high biological diversity in a heterogeneous of estuarine habitats or ecological subsystems environment. Our main goal was to advance the under- (Yáñez-Arancibia and Day, 1988). Prevailing standing of linkages between environmental dynamics in winds, littoral currents and the discharge of rivers tropical coastal areas and flatfish movements to utilize induce a net inflow through the east inlet (Puerto estuarine plume influenced areas as part of their life cycles. Real) and a net outflow through the west inlet The general objective of this study is to present a (Carmen). The net inflow creates elevated salinity comparative analysis of the ecological strategies of two conditions and sandy sediments in the northeast dominant marine flatfish species associated with estuarine part of the lagoon. The highest river discharge P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185 175

Fig. 1. The Campeche Sound region showing the net flow of the circulation pattern in the two inlets (e.g., Puerto Real & Carmen) connecting the sea shelf with Terminos Lagoon. The dynamics of the estuarine plume from the Grijalva/Usumacinta mega-delta (which includes Terminos Lagoon), results in a significant contribution of organic matter and terrigenous sediments from the coastal plain and estuarine waters to the continental shelf in the Southern Gulf of Mexico.

occurs in the southwest part of the lagoon, its ecological interactions with the shelf lead to creating conditions of low salinity, and turbid estuarine plume conditions on the inner sea shelf waters rich in nutrients. This estuarine system and (Day et al., 2003; Yáñez-Arancibia et al., 2004).

Fig. 2. Seasonal patterns of environmental parameters in the study area, showing the seasonal parameters in shallow shelf waters which define the three climatic seasons; Dry season (February-May), Rainy season (June-Sept/Oct) and Nortes season (October-February). These climatic sequences control seasonal pulses in ecosystem dynamics including temperature and salinity gradients, and the detritus biomass in the estuarine plume. 176 P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185

C) The dynamics and net flow between the two broad estuarine plume. The mixed waters of the estuarine estuarine inlets that connect Campeche Sound plume have a shorter residence time compared with semi- with Terminos Lagoon (Fig. 1) results in a strong arid tropical lagoon systems, and this is especially true contribution of primary productivity from estuar- during periods of high river discharge. These conditions ine waters to the adjacent continental shelf via increase the discharge of nutrients and riverine silts particulate organic matter (detritus) from a variety through estuarine inlets to the inner continental shelf of sources, including phytoplankton (Soberón- (Day et al., 2003; Yáñez-Arancibia et al., 2004). Chávez et al., 1988), mangroves (Day et al., Aquatic primary productivity inside Terminos Lagoon 1997), and riverine influence averaging about is highest during the wet and nortes seasons (from July 4470 m3/sec (Day et al., 2003; Yáñez-Arancibia through November), and declines during the dry season et al., 2004). The contribution of primary (December to April) (Day et al., 1988). The peak in producers (Rojas Galavíz et al., 1992), and the primary productivity in the lagoon occurs in November circulation pattern in the estuarine inlets (Yáñez- (equivalent to 325 g Cm-2 yr-1) during the early nortes Arancibia et al., 1991; David and Kjerfve, 1998) and late river discharge season, a period of with moderate produces a strong seasonality of detrital biomass, turbidity and low solar radiation (due to cloud cover), but and its availability in the inner sea shelf via the with the highest nitrate and phosphate levels from river estuarine plume with higher levels of organic inputs. The net flow from east to west in the lagoon matter just outside of Carmen Inlet during March- results in a strong export of organic matter and nutrients April (dry season), and outside of Puerto Real in to Campeche Sound through Carmen Inlet from October June-July (rainy season). until April. Thus, the patterns of lagoon primary D) The ecological interactions between Terminos production, rainfall, river discharge, and lagoon circula- Lagoon and Campeche Sound (Yáñez-Arancibia tion determine the seasonality of availability of organic et al., 1985) and the main sedimentary provinces in detrital biomass on the inner shelf (Fig. 2). the southern Gulf of Mexico shelf (Yáñez- These processes are extremely important in main- Arancibia and Day, 1988) produce two different taining the salinity gradients, appropriate temperatures, habitats on the inner shelf. The western part (in and nutrient and organic matter levels that lead to a front of Carmen Inlet) is strongly influenced by predictable environment, which in turn is thought to fresh and estuarine waters with prevailing terrige- regulate biological processes and conditions for recruit- nous sedimentary facies, and the eastern part (in ment of estuarine-dependent and estuarine-related front of the Puerto Real Inlet) has typical marine species (Yáñez-Arancibia and Pauly, 1986; Yáñez- conditions with prevailing calcium carbonate Arancibia et al., 1991, 1994; Day et al., 1995, 1997; sedimentary facies. Yáñez-Arancibia et al. Sánchez-Gil and Yáñez-Arancibia, 1997; Lara-Dom- (1991), gives a detailed description of the inlet ínguez et al., 1993, Lara-Domínguez, 2001; Jones et al., areas. 2002; Baltz and Jones, 2003).

2.2. Environmental dynamics and main pulses in the 3. Species characteristics study area Etropus crossotus Jordan & Gilbert: The general The main ecological processes that control produc- distribution of the fringed flounder is from Chesapeake tivity in the southern Gulf of Mexico are river discharge, Bay, all of the Gulf of Mexico and the Caribbean Sea productivity of wetlands, sediment type and climate including the Antilles through Brazil. In the southern (Yáñez-Arancibia and Day, 1988; Day et al., 1997). Gulf of Mexico, it frequently occurs in the shrimp These forcings are not constant but occur as energetic grounds of Farfantepenaeus aztecus and Litopenaueus pulses on different temporal and spatial scales (Fig. 2). setiferus (Yáñez-Arancibia and Sánchez-Gil, 1986). In Day et al. (1995, 1997), and Yáñez-Arancibia et al. Campeche Sound, the fringed flounder has a broad (2004) discuss how these seasonal pulses produce distribution in shallow water over a variety of bottom benefits on different ecological scales and how they sediment types, ranging in size from 5 to 14 cm, with the are integrated into the functional structure of the coastal smallest individuals present during October (nortes area in the Gulf of Mexico. season) (Yáñez-Arancibia and Sánchez-Gil, 1986). Estuarine systems dominated by high riverine input There is a relationship between size-frequency distribu- like Terminos Lagoon have a strong impact on the tion and salinity. In general, juveniles occur in estuarine continental shelf in terms of a large flood tide delta and a systems, and adults in adjacent marine waters. Inside P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185 177

Table 1 Distribution of data collected for the two flatfish species Total Dry season Rainy season Nortes season (February – May) (June – September) (October – January) Depth (m) b20 20–40 N40 b20 20–40 N40 b20 20–40 N40 Number of tows 128 25 7 9 35 20 6 19 5 2 E. crossotus (n) 1060 277 46 51 364 30 10 185 97 0 Abundance (gr) 11050.9 2349 813.6 237.3 4734 6380 61.8 1316 960 0 C. spilopterus (n) 420 90 27 59 68 105 5 63 3 0 Abundance (gr) 6665.3 1013 304.5 967.2 1880 1697 92.5 662.3 48.8 0

Terminos Lagoon, this species is frequently found in frequently found on the shrimp grounds of Farfantepe- turbid estuarine waters and marine influenced areas, naeus aztecus and Litopenaueus setiferus. In Campeche occasionally in very low salinity areas, and as a cyclical Sound, Yáñez-Arancibia and Sánchez-Gil (1986) reported visitor in zones of Thalassia testudinum (Yáñez- than the bay whiff occurs on a variety of bottom sediment Arancibia et al., 1988). Reichert (1998) reported that in types, with a preference for silt-clay. They observed sizes of the south Carolina coast 50% of females E. crossotus individuals from 6.6 to 17.7 cm, with the smallest reached maturity at 8 to 8.5 cm, and could grow to that individuals occurring during the nortes season (October). size within one spawning season. For the same area, In Terminos Lagoon, this species frequently occurs as a Reichert (2003) indicated that food of fringed flounder cyclical visitor in low salinity areas, and as a frequent consisted of zooplankton and epibenthic organisms, with resident in the Carmen estuarine inlet (Yáñez-Arancibia no clear ontogenetic shift in prey with increasing fish et al., 1988). The bay whiff is a third order consumer size. In marshes of Guaratuba Bay, Brazil, E. crossotus feedingmainlyonsmallfish,and epibenthic fauna, mostly feeds upon gammarids amphipods, small fishes, gastro- decapods (Castillo-Rivera et al., 2000). These authors pods and polychaetes (De Tarso et al., 1998). reported that in contrast with fringed flounder, the bay whiff Citharichthys spilopterus Gunter: The distribution of the has significant ontogenetic differences in diet and trophic bay whiff is from New Jersey, all of the Gulf of Mexico and niche breadth. Similarly in marshes of Guaratuba Bay, the Caribbean Sea, including the Antilles through Santos, Brazil, C. spilopterus feeds mainly on carideans and small Brazil (Yáñez-Arancibia and Sánchez-Gil, 1986). Along fishes (De Tarso et al., 1997, 1998) but it has different the Mexican Gulf coast from Veracruz to Campeche, it is preferences throughout its life stages.

Fig. 3. Spatial distribution of relative abundance for the two flatfish species Etropus crossotus and Citharichthys spilopterus. The seasonal changes of a. gr/m2 and b. ind/m2 in three different depth strata on the sea shelf, indicates the migration patterns and coastal habitat utilization of the species in a sequential use in time and space. 178 P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185

4. Data sources and methodology 3.7 cm. Tows were 30 minutes each, at 2.5 knots covering an average area of 21,182 m2 per tow. Sampling depth The data were taken in Campeche Sound from random varied from 10 m in the area of estuarine plume influence stratified research surveys during the period 1978-1985, in off Terminos Lagoon (proximal to the two estuarine inlets a total of 128 samples from 110 different locations. Fish Fig. 1), to 100 m on the continental shelf (Yáñez-Arancibia were collected with a shrimp trawl with a mesh size of and Sánchez-Gil, 1986). A total of 1060 individuals of

Fig. 4. A. Seasonality of size distribution for Etropus crossotus. The monthly length distrubution and fitted growth curve permit an understanding of the recruitment pattern. E. crossotus uses the estuarine-shelf system as an estuarine-related species. B. Seasonality of size distribution for Cithar- ichthys spilopterus. The monthly length distribution and fitted growth curve permits an understanding of the recruitment pattern. C. spiloterus uses the estuarine-shelf system as an estuarine-dependent species. P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185 179

E. crossotus and 420 individuals of C. spilopterus were these environmental pulses and the strong seasonality of collected (Table 1). detrital biomass, and its availability in the inner sea shelf via the estuarine plume, the seasonally of the estimated 4.1. Species analysis recruitment patterns were compared in time and space. This allowed us to identify and suggest some mechan- For comparative analysis of spatial and temporal isms acting on the recruitment processes. We assumed variations in the abundance of both species, we that the seasonal patterns are repeated each year. measured changes in relative abundance (gr/m2 and ind/m2) during: a) the three climatic seasons; rainy, dry 5. Results and nortes; and, b) in three bathymetric strata defined as estuarine plume b20 m, 20-40 m, and marine waters 5.1. Distribution and abundance N40 m depth, based on Yáñez-Arancibia et al. (1991, 2004, Table 1). Fig. 3a shows that, for E. crossotus, the highest A total of 789 individuals of E. crossotus, and 355 abundance occurs during the rainy season (20-40 m) and individuals of C. spilopterus, were used to estimate the the lowest during nortes season in deep waters (N40 m growth parameters of the von Bertalanffy equation using depth). The abundance pulse in the rainy season is the Electronic Length Frequency Analysis ELEFAN-I attributable to few individuals, but with large sizes (Pauly and Morgan, 1987) implemented in the FAO (N11 cm) (Figs. 3b and 4A). The opposite occurs in ICLARM Stock Assessment FISAT software (Gayanilo nortes season, when the presence of many individuals in et al., 1993). Samples were grouped as monthly length 20-40 m but of small sizes (b9 cm) was observed. A frequency distributions in an artificial year, assuming no more widespread distribution occurred during dry major changes between years. The FISAT routines for the season from b20 m to N40 m depth. Fig. 4A shows quantitative estimation of seasonality of recruitment were that fringed flounder were most abundant as adults used beginning with early juveniles, as suggested by (N11 cm) during dry and rainy seasons, and small Pauly (1982), and the derivation of recruitment from the juvenile's abundance was highest in the nortes season. length frequency data for tropical demersal communities For C. spilopterus the highest abundance occurred as described by Pauly and Navaluna (1983). Sánchez-Gil during the dry season, and the lowest during nortes and Yáñez-Arancibia (1986), Pauly and Yáñez-Arancibia season, both in deep waters N40 m depth (Fig. 3a). (1994) considered recruitment as the key difference During the rainy season, the highest abundance was in between “estuarine dependent” and “estuarine related” intermediate depth waters (20-40 m), and during the nekton strategies. If recruitment occurs inside the estuary, nortes season, abundance was concentrated in shallow the species are estuarine-dependent, and if recruitment water b20 m. Fig. 4B shows that the bay whiff was most occurs in the estuarine plume on inner sea shelf, the abundant as adults (N12 cm) during rainy and nortes species are estuarine-related. seasons, while the abundance of small juveniles was In order to understand the relationship between the high all year. biological and ecological strategies of each species and the detailed description of the estuarine-shelf dynamics 5.2. Biological parameters and recruitment by Yáñez-Arancibia et al. (1991), the environmental variables of Fig. 2 were considered to characterize the The parameters estimated for the two species are estuarine influence onto the shallow continental shelf. presented in Table 2,andFig. 4A and B. The results show Based on the discussion by Day et al. (2003), Yáñez- that the two species have very similar patterns of growth. Arancibia et al. (2004), about the sequence in time of The M and Z values indicated that both are annual species

Table 2 Summary of length data analyzed for the studied species Total Dry season Rainy season Nortes season Month 2 3 4 5 6 7 8 9 10 11 1 E. crossotus (n) 789 92 36 32 6 14 27 331 38 98 115 Mean Length (cm) 5–20 7–14 10–20 10–13 6–15 9–14 5–12 5–14 9–16 5–13 6–16 C. spilopterus (n) 355 75 90 11 18 37 31 27 22 10 34 Mean Lesngth (cm) 5–21 6–15 9–21 6–95–14 8–18 11–14 9–16 12–18 5–13 5–19 180 P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185 of rapid growth, with values of K of 0.46 and 0.42 for recruitment occurs during the nortes season from Decem- fringed flounder and bay whiff, respectively, reaching a ber to February. However, Fig. 4B shows that small sizes Lθθ around 22 cm for both species. In the case of fringed occur all year. flounder, a C value of 0.3 implies weak seasonal To explain the tendency of recruitment patterns, oscillations of growth and the “winter point” (WP) different sections of Fig. 5 show an apparent relation- value of 0.08 indicates that in this part of the year ship of both species with the environmental dynamics (January) growth is most reduced. For the bay whiff, the and main pulses in the study area. The first recruitment value of C=0 implies no seasonal oscillation; and no pulse of E. crossotus (October-December) starts during clear variation of growth during the year, WP=0. The the major estuarine discharge from Terminos Lagoon to result of t0 is consider as “a chronological magnitude” the sea shelf. This discharge produces lower salinity and between 0.1 to 1 in a year, and not as an absolute age. temperature in the estuarine plume areas, and high With these results and those of the FISAT program, detrital biomass on the western part of inner shelf, via we estimated the tendency of recruitment patterns estuarine flushing through Carmen inlet. These parti- shown in Fig. 5. Fringed flounder has two recruitment cular conditions of the estuarine plume are maintained in pulses, both of which occur during the nortes season, the the area during the nortes season. The second recruit- main pulse occurs at the beginning of the nortes ment pulse begins in February during the period of high (October-December); and the second at the end of the detrital biomass on the eastern inner shelf (off Puerto nortes-early dry season (February-April). Thus the peak Real inlet), lasting until April during the dry season, in abundance of this species during nortes season in the after which temperature and salinity rapidly increase shallow waters of the estuarine plume is comprised of (Figs. 2 and 5). The principal recruitment pulse of C. individuals of small sizes (Figs. 3b and 4A). spilopterus starts just after the decrease in abundance of Fig. 5 shows that C. spilopterus has continuous the fringed flounder (April). Bay whiff recruitment recruitment in two pulses; the largest of which occurs occurs in between the two main fluxes of detrital from April to August (dry-rainy season). A smaller biomass originating in the estuarine plume, which continues until the beginning of the rainy season, after which strong estuarine discharge begins again (Figs. 2 and 5). It is clear that both recruitment pulses of E. crossotus occur during the nortes season when there are estuarine conditions, including lower salinity (12.6 to 25.3psu) in the shallow waters of the shelf. For C. spilopterus, the major pulse occurs during higher salinity marine conditions in the estuarine plume areas (27 to 29.3 psu) without the influence of the nortes season (Figs. 2 and 5). However for both species, the importance of seasonal dynamics of the estuarine plume is evident, particularly with respect to the flux of detritus towards the shelf from the Terminos Lagoon system. It is important to point out that both species are secondary consumers and they do not feed directly on detritus, but optimize the availability of detritus-dependent benthic epifauna to secure food availability during recruitment.

6. Ecological strategies: A comparative analysis

Table 3 summarizes the information we used as a framework for the comparative analysis in this paper, Fig. 5. The seasonal recruitment patterns for Etropus crossotus and and illustrates the main differences between species life Citharichthys spilopterus show a coupling with the seasonality of the cycles. This analysis permits us to describe the life main environmental parameters which characterize the estuarine plume in the study area. In both cases, recruitment takes place as a sequential history patterns of fringed flounder and bay whiff in the process that is driven by seasonality in estuarine plume dynamics, area, and to resolve the linkages between ecological suggesting that seasonal programming is an important strategy. strategies and environment in juveniles at his tropical P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185 181

Table 3 Comparative analysis of the different parameters observed for both species Etropus crossotus Citharichthys spilopterus Spatial distribution Estuarine plume areas, in all type of silts, Estuarine plume to marine areas, mainly silt-clay (Yáñez-Arancibia and related to shallower waters from b20 up to 40 m. sediments, with broad depth distribution from Sánchez-Gil, 1986) b20 to N40 m. Temporal distribution No marked temporal variation of relative abundance. Marked temporal variation of relative abundance. (abundance) (this study) A main pulse of abundance during rainy season, Two main pulses of abundance; one during rainy in waters from 20-40 m. season in depths 20-40 m; and other during dry season in N40 m. Size distribution (this study) Ranges from 5 at 20 cm. High frequency of small Range from 5 at 21 cm. High frequency of small sizes sizes (b9 cm) during nortes season. High frequency (b10 cm) during all seasons. High frequency of large of large sizes (N11 cm) during rainy and dry season. sizes (N12 cm) during nortes and rainy season. Concentration of small and large sizes in shallow Concentration of small and large sizes in shallow waters waters during rainy season. during nortes season. Growth parameters (this study) Lθθ=22 cm; K=0.46 (1/year); C=0.3 WP=0.08, Lθθ=21.8 cm; K=v0.42 (1/year); C=0, WP=0, M=1.17 (1/year), t0=0.74 and Z=1.64 year. M=1.11 (1/year), t0=0.24 and Z=1.25 year. Reproduction One long period from May to November mainly Two short periods. In the rainy season from Aug to (Yáñez-Arancibia and during rainy season. Estuarine plume from October and in the dry season from February to April. Sánchez-Gil, 1986) b20 to 40 m to depth. Estuarine plume b20 m depth. Recruitment (this study) Two important pulses in the same climatic season Two pulses; the main from April to August (dry-rainy) (nortes). From October to December and from il the estuarine plume and the secondary from February to April, both related to the highest detrital December to February in the nortes season, inside biomass in the estuarine plume (20-40 m). Terminos Lagoon. Both pulses related to the highest Estuarine-related species. detrital biomass in the estuarine plume. Estuarine- dependent species. Use of Terminos Lagoon Occasional visitor in clear water areas of Thalassia Permanent resident in high turbidity areas near (Yáñez-Arancibia et al., 1988) beds, near Puerto Real inlet. Feeding purposes. Carmen inlet. Nursery purposes. Food habits Second order consumer which feeds mainly on Second order consumer which feeds mainly on benthic (De Tarso et al., 1997, benthic epifauna and small amount of organic epifauna. Different food habits of juvenile and adults. 1998; Castillo-Rivera, detritus. Similar food habits of juvenile and adults. Juveniles feed mainly on copepods and peracarids, et al., 2000; Reichert, 2003) adult's main food is fishes. coastal area. This, coupled with the movements of these this season that the species visits the lagoon, where sizes two flatfishes, demonstrates how these species utilize from 5 to 15 cm have been observed in areas of marine estuarine plume influenced areas as part of their life influence in Thalassia testudinum beds (Yáñez-Aranci- cycles. A brief narrative of our interpretation of this bia et al., 1988, 1993). These authors refer to E. information is given next. crossotus as an occasional visitor to Terminos Lagoon, Throughout the year, Etropus crossotus occurs in for feeding purposes. waters of 20-40 m, where it spends most of its life cycle Citharichthys spilopterus, in contrast to E. crossotus, using areas influenced by the estuarine plume (Fig. 3a exhibits marked seasonal variations in abundance within and b). During the early rainy season, adults move to the estuarine plume, as well as in marine areas of the shallow waters b20 m for a protected spawning period continental shelf, due to seasonal migrations (Fig. 3a). Is as shown in Fig. 3b. This coincides with a great possible to relate the pulse of adult abundance during the abundance of larval stages of fringed flounder as has rainy season with the main spawning period, which been reported by Flores-Coto et al. (1991) in the same apparently occurs in shallow waters of the continental shallow waters later during spring, and the long shelf in b20mto40m(Fig. 3b), and likely produces the reproduction period of this species is from May to recruitment pulse during nortes (December-February) November (Flores-Coto et al., 1992). It is possible that described in this study. We observed high concentra- fringed flounder also use waters from b20 to 40 m as tions of bay whiff juveniles in the shallow waters during nursery and recruitment grounds, because the highest nortes (Fig. 3b), however the recruitment peak is less frequency of small sizes occurs during nortes (Figs. 3b evident (Figs. 4B and 5), suggesting that recruitment and 4a), which confirms the estimated recruitment occurs inside Terminos Lagoon. To support this patterns in this study (Fig. 5). During the dry season, it is conclusion, we consider the information of Yáñez- possible to observe juveniles and adults in the study Arancibia et al. (1985) who reported a high frequency area, mainly of sizes N11 cm, and it is probably during and density of bay whiff juveniles inside the lagoon, for 182 P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185 nursery purposes, particularly during the nortes season in highly repetitive between seasons, making the fish low salinity areas, and they considered this species as a population gradually more dependent on the estuarine permanent resident of Carmen Inlet. A similar pattern system for the maintenance of high biomass. In addition, was reported by Walsh et al. (1999) in estuaries of North utilization of estuarine resources may diminish the Carolina, where the highest density of flatfishes was in likelihood of a mismatch between seasonal prey produc- the upper estuary, and C. spilopterus was characterized tion on the shelf and production of prerecruits, thus by juveniles associated with muddy sediments. The reducing the likelihood of a failed year class attributable to largest fishes in that area were in the lower estuary, where match/mismatch predator-prey dynamics (Cushing, they occurred in channels and in areas of sandy 1995). sediments. We observed a secondary pulse of abundance In the present study, the seasonal programming in deeper waters during the dry season (N40 m) (Fig. 3a between the two species of flatfishes is clear (Fig. 5 and and b), showing that the migration from the estuary to the Table 3). Both species use the inner shelf for reproduc- shelf is size-dependent, and may be related to a second tion and recruitment. Nevertheless, they reduce compe- period of reproduction. This leads to our conclusion that tition for environmental resources in several ways: a) the main recruitment peak is on the shelf (20-40 m) they occupy different depth strata during reproduction; towards the end of the dry season into the rainy season b) they exhibit a different seasonality of reproduction; c) (April-August) (Fig. 5). After this, adults move into they use different habitats for feeding in the inner marine waters N40 m, which serve as maturation areas, as lagoon; d) they exhibit differences in seasonality of has been reported by Yáñez-Arancibia and Sánchez-Gil recruitment periods; e) they use different habitats for (1986), completing the life cycle. recruitment grounds (C. spilopterus); and, f) they have The above information indicates that the two species of different food habits at different sizes (C. spilopterus). flatfishes possess spatial and temporal strategies for using In the habitats of Terminos Lagoon, a similar phe- coastal habitats throughout the year (Figs. 3, 4 and 5). Even nomenon was discussed by Yáñez-Arancibia et al. (1993, though the two flatfish species behave similarly, they are 1994). They mentioned that in these habitats, it is the temporally out of phase as related to the main environ- juveniles of fish populations, and not the adults, that exert mental pulses in the estuarine plume, and segregate the greatest pressure on the food supply (Cowan et al., spatially via the alternation of recruitment grounds of C. 2000). This point, apparently not made in the extensive spilopterus inside the estuary. E. crossotus spends most of literature on lagoons and estuaries, provides an objective its life cycle in shallow waters, while C. spilopterus carries criterion for referring to estuaries and estuarine plume out seasonal migrations. Also the recruitment patterns of systems as critical habitats, mainly in tropical regions. these species have a seasonal programming related to the The results suggest that fish migration to shallow environmental variability of the region (Fig. 5). waters also allows optimum utilization of food availability Adaptation to seasonal variations in abiotic para- during recruitment, mainly the epibenthic fauna which meters, food supply, and competition results in the utilize the seasonality of detrital biomass pulses. We phenomenon called seasonal programming. This refers believe that the main differences between patterns of to the temporal and spatial sequence of lagoon-shelf relative abundance for the two flatfish species are habitat utilization by juvenile and pre-adult fishes (Yáñez- controlled by the seasonality of the estuarine discharge Arancibia et al., 1988, 1994; Pauly and Yáñez-Arancibia, and detrital biomass availability on the inner shelf (b20 m) 1994), and has been discussed for species utilizing (Fig. 5). Nutrient inputs, primary production and fisheries Terminos Lagoon by Yáñez-Arancibia et al. (1986, yields are positively correlated in estuaries and coastal 1994);andYáñez-Arancibia and Lara-Domínguez systems (Nixon et al., 1986; Iverson, 1990; Houde and (1988). These studies indicated that for a given species, Rutherford, 1993; Caddy, 1993). From a statistical point of seasonal programming implies that its representatives view, Govoni et al. (1989); Govoni (1997) analyzed (mainly juveniles) feed, in the course of their ontogeny, on menhaden recruitment in association with the Mississippi a succession of different food types, often gathered from Riverforanumberofyearsandconcluded,asinour different sub-areas within a given lagoon. Similarly, in a results, that recruitment was elevated with increased river recent study of sympatric juvenile tongue fishes (gen. discharge to the coastal zone, possibly as an indirect Symphurus)inaLouisianaestuary,Switzer et al. (2004) response to increased primary production stimulated by demonstrated strong size related shifts in resource enhanced nutrient flux into the area. utilization along estuarine environmental gradients asso- Cury and Roy (1989), Cury and Pauly (2000) discussed ciated with differences in micro habitat. This sequential the existence of an optimal environmental “window” for utilization of food types and feeding locations may be fish recruitment. They concluded that the patterns between P. Sánchez-Gil et al. / Journal of Sea Research 59 (2008) 173–185 183 fish recruitment (the dome-shaped relationship of the of recruitment patterns of the two species of flatfish optimal environmental window) and the spatial fish permits classification of E. crossotus as an estuarine- reproductive strategies coupled with the environment related species and C. spilopterus as an estuarine- appear to be consistent among fish species. In this study we dependent species. conclude that the contribution of primary production (as 6. The maintenance of hydrological functioning of measured by organic matter in sediments) from estuarine estuarine inlets, which is key to estuary – shelf waters to the adjacent continental shelf, the persistence of interactions (e.g., Terminos Lagoon-Campeche estuarine conditions on the inner shelf as a result of the Sound), is required to assure the fertility of continental extension of the estuarine plume, and the seasonality of shelf waters and associated fish resources. This will interactions between Terminos Lagoon and Campeche preserve salinity gradients, nutrient contributions, and Sound, produce the characteristics which drive flatfish habitat diversity that regulate biological processes and ecological strategies. Thus, by observing recruitment condition estuarine dependency of species recruitment. patterns of different species, it is possible to understand the relationship between tropical flatfish species in the Acknowledgements southern Gulf of Mexico and the influence of estuarine plume of the Grijalva-Usumacinta mega delta. Data support was provided by the Project: “Fishery and Ecological Atlas of the Southern Gulf of Mexico”, 7. Conclusions funded by the EPOMEX Program (from 1990 to 1997, chaired by the senior author), with technical assistance of 1. Given the high diversity that characterizes tropical the ICLARM-Philippines through Dr. Daniel Pauly (at regions, the study of “dominant species” has been a present Director of the Fisheries Centre, University of widespread research strategy. In our opinion, this British Columbia, Canada). This paper is a joint activity approach can identify important ecological interactions under the Agreement of Understanding between Louisi- among members of a diverse demersal fish community. ana State University USA, and Instituto de Ecologia A. C. These typical species characterize the structure and Mexico, Sub-agreement School of the Coast & Environ- function of the high diversity communities, acting both ment LSU, and Coastal Ecosystems Unit INECOL. Part as sources of information of the species themselves, and of the data analysis was with the support of Louisiana Sea of other species with similar behavior. Grant Program, NOAA, Grant No. 16RG2249. 2. Differences in seasonal programming between the two species of flatfish are clear. They reduce competition References for resources in several ways: a) they utilize different depth strata during reproduction; b) they exhibit Baltz, D.M., Jones, R.F., 2003. Temporal and spatial patterns of different seasonality of reproduction; c) they use microhabitats use by fishes and decapods crustaceans in a Louisiana – different habitats for feeding in the inner lagoon; d) estuary. Trans. Am. Fish. Soc. 132, 662 678. Caddy, J.F., 1993. Towards a comparative evaluation of human they exhibit differences in the seasonality of recruit- impacts of fishery ecosystems of enclosed and semi-enclosed seas. ment; e) they utilize different habitats for recruitment Rev. Fish Sci. 1, 57–95. grounds (C. spilopterus); and, f) they have different Castillo-Rivera, M., Kobelkowsky, A., Chávez, A.M., 2000. Feeding food habits at different sizes (C. spilopterus). biology of the flatfish Citharichthys spilopterus (Bothidae) in a – 3. There exist strong links between environmental tropical estuary of Mexico. J. Appl. Ichthyol. 16 (2), 73 78. Cowan Jr., J.H., Rose, K., De Vries, D.R., 2000. 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