Vertical segregation of two species of Hyphessobrycon ( Characiformes : Characidae ) in the Cabiúnas coastal lagoon , southeastern Brazil

Segregation in the use of the water column by two congeneric species of Characidae, Hyphessobrycon bifasciatus and H. luetkenii, was investigated through underwater observations in the Cabiúnas coastal lagoon in northeastern Rio de Janeiro, Brazil. The use of the water column by the two species differed significantly. Hyphessobrycon luetkenii occupied mainly the uppermost stratum, with 79% of the observations within 20 cm of the surface; whereas H. bifasciatus was more common between 20 cm and 40 cm below the surface (55% of the observations). Predation pressure, macrophyte cover and nutrient distribution may influence this vertical segregation.

The use of space seems to be the main factor explaining species richness and community structure (MacArthur, 1958;Schoener, 1974Schoener, , 1983;;Cunha & Vieira, 2004 and references therein).Differences in the pattern of use of space are especially important in complex or three-dimensional environments, and their study is a basic requisite for understanding species coexistence.Studies of the use of microhabitats by fish in lotic ecosystems suggest that depth, substrate composition, and water velocity determine the distribution of species (Daniels, 1987;Grossman et al., 1987;Bührnheim, 1999;Rincón, 1999).In lentic freshwater systems, the spatial distribution of fish is influenced in pelagic zones by factors associated with depth, such as temperature, light, dissolved oxygen, food type, and food abundance (McKaye, 1977;Seehausen & Bouton, 1997); and in the littoral and demersal zones by microhabitat heterogeneity (Diehl & Eklöv, 1995).Ross (1986) reviewed different fish communities and taxa levels, and showed that spatial segregation is the main factor that explains the coexistence of phylogenetically related fishes.Studies on fish communities have shown that use of space or microhabitats distinguish species, often congeneric ones; whereas other dimensions of the ecological niche, such as diet and morphology, may overlap considerably (see Bouchon-Navaro, 1986 for reef fishes; Kohda & Yanagisawa, 1992 for lake cichlids; Ornellas & Coutinho, 1998 for marine-grass inhabitants; Nico & Thomerson, 1989 for annual killifishes;and Sabino & Zuanon, 1998 for Amazon stream fishes).Differentiation in microhabitat use is a key factor structuring fish communities (Junk et al., 1983;Fernandes, 1997;Bührnheim, 1999;Rincón, 1999).
The coastal lagoons of Parque Nacional da Restinga de Jurubatiba (PNRJ) in Rio de Janeiro State, Southeastern Brazil, have a rich macrophyte community supporting a great variety of microhabitats (Henriques et al., 1988;Esteves, 1998).We assume that differentiation in the use of space could be an important factor in structuring the fish communities of these lagoons, allowing closely related species to coexist.In PNRJ lagoons, the genus Hyphessobrycon Durbin is represented by two species, H. bifasciatus Ellis, 1911 andH. luetkenii (Boulenger, 1887), which occur together only in Cabiúnas Lagoon.We made direct observations by snorkeling to investigate water column use by these species in Cabiúnas Lagoon.
The Restinga de Jurubatiba National Park is located in the northeastern part of Rio de Janeiro State, Brazil, between 22 o 17'-22 o 18' S and 41 o 39' -41 o 40' W (Fig. 1).The climate is tropical ("AW" in the Köppen classification), with rainy periods in summer and dry periods in winter (Henriques et al., 1988).The fish community of seven coastal lagoons of the park is composed of 39 species, and species of Hyphessobrycon occur in four (Caramaschi et al., 2004).Cabiúnas Lagoon has an area of 0.34 km 2 and 2.37 m mean depth (Panosso et al., 1998).The community of aquatic macrophytes harbors 15 species in the nearshore parts of the lagoon (Henriques et al., 1988).In this area, the stands were dominated by the submersed macrophyte Potamogeton stenostachys K. Schum.and the emergent Typha domingensis (Pers.)Kunth.The members of Hyphessobrycon are usually found in the marginal areas of the lagoon, where the depth does not exceed 1.20 m and there are dense macrophyte stands.Three stands of macrophytes with similar composition were used in the study (Fig. 1).
The fish were observed during daylight by snorkeling dives on April 27, 2003, and from April 8 to 10, 2004.To assess the use of water column by one of the species when the other was absent, additional snorkeling observations were made in Carapebus Lagoon, where only H. bifasciatus occurs (Caramaschi et al., 2004).Each observation session lasted for five minutes, and was based on a focal individual approach (sensu Altman, 1974).Observers (AAC, SMQL, and JISB) remained in the same place during the diving sessions.swimming, or not, with the other species of Hyphessobrycon, in the same visual field.The significance of the differences in frequency of each category within each variable between species was tested with one-tailed chi-square tests and Yates correction when necessary, assuming as significant values of P < 0.05 (Zar, 1984).We recorded the presence of individuals of other fish species, their identity, position in water column, and the occurrence of agonistic behavior.Voucher specimens of H. bifasciatus and H. luetkenii were deposited in the collection of the Laboratório de Ictiologia Geral e Aplicada, Universidade Federal do Rio de Janeiro (UFRJ 7284-7287).
In Cabiúnas Lagoon, we observed 185 individuals of H. luetkenii and 180 of H. bifasciatus in 74 dive sessions, totaling more than six hours of underwater observations.Patterns of water-column use differed significantly (Fig. 2a).Hyphessobrycon luetkenii occupied mainly the upper strata, with 79% of the observations within the uppermost 20 cm, 20% in the second stratum, and less than 1% below a depth of 40 cm.Individuals of H. bifasciatus were more common between 20 cm and 40 cm (55% of the observations), and less frequent toward the water surface (29%) and lagoon bottom (16%) (Fig. 2a).
The species did not differ significantly in foraging tactics (Fig. 2b), feeding mainly on items in the water column (76% and 54% of the observations for H. bifasciatus and H. luetkenii, respectively, Fig. 2b).
The intraspecific social organization differed between the two species (Fig. 2c).Hyphessobrycon luetkenii swam primarily in groups of 2-5 individuals (51% of the observations), whereas individuals of H. bifasciatus were more frequently (54%) observed alone.Groups with more than five individuals were less frequent for both species (approximately 10%, Fig. 2c).Syntopy was recorded in 38% and 19% of the observations of H. luetkenii and H. bifasciatus, respectively (Fig. 2d).
No agonistic behavior was observed between the species of Hyphessobrycon.The associated fish fauna was composed of Poecilia vivipara (Poeciliidae) at the surface and Geophagus brasiliensis (Cichlidae), Hoplias malabaricus (Erythrinidae), and Oligosarcus hepsetus (Characidae) at the bottom.The latter was occasionally observed attacking H. luetkenii from bottom to surface, in our above-surface observations, between diving sessions.
In Carapebus Lagoon, we observed 138 focal individuals of H. bifasciatus in 24 diving sessions, totaling two hours of underwater observation.All individuals were observed below 40 cm and in small groups (45% of the time with five or fewer individuals, 43% of the time alone, and only 12% in larger groups), and foraging among the macrophytes (83% versus 17% in the water column).
Vertical segregation in the use of space seems to allow different species to coexist in complex three-dimensional environments such as freshwater ecosystems (see Sabino & Zuanon, 1998;Esteves & Aranha, 1999, and this study).The syntopic species of Hyphessobrycon clearly segregate from each other in the water column in Cabiúnas Lagoon.Similar patterns of vertical segregation have been observed for other congeneric fish species (Mendelson, 1975;Surat et al., 1982;Moyle & Senanayake, 1984, Aranha et al., 1993).
Both species are suspension feeders, and available data on their diets suggest that they are generalists (Aguiaro & Caramaschi, 1998).Microhabitat structure may influence the differential use of the water column by the two species.The macrophyte stands where the observations were made in both lagoons were dominated by Potamogeton stenostachys and Typha domingensis.However, the richness and structure of macrophytes can differ with depth in Cabiúnas Lagoon, as suggested by Henriques et al. (1988).Preferences to use the interface of open area and thickly vegetated areas, or the inner spaces of the macrophyte stands should be evaluated experimentally.In this approach, preferential use of the water column by H. luetkenii may be evaluated by experimentally excluding H. bifasciatus.Likewise, the availability of resources such as suspended particles, which were not measured during this study, may vary with depth (Spence, 1967) and thus influence the distribution of the two species throughout the water column.
Hyphessobrycon bifasciatus, even when living without the presence of the congeneric H. luetkenii as in Carapebus Lagoon, still occupies the lagoon bottom.This suggests, as established in previous studies (Ross, 1986;Peres-Neto, 1999;Casatti et al., 2005), that the use of habitat and microhabitat per se, rather than competition, must be the main factor in resource partitioning between fish species.
Predation is another factor that must affect the distribution of Hyphessobrycon species in these coastal lentic environments.Power (1984) demonstrated the importance of aerial predation in modifying the vertical pattern of fish distribution in a clear tropical stream.Ardeidae birds are commonly seen foraging in the PNRJ lagoons (Alves et al., 2004), but there are no studies on diet or hunting behavior of birds in southern Brazilian coastal lagoons.However, Carvalho & Del-Claro (2004) studying the effects of the avian predation pressure on Hyphessobrycon eques suggested that the avoidance of the surface by the fishes in the presence of a predator could be an evolutionary response to this pressure.It could also explain why H. bifasciatus occupies only the lagoon bottom even without H. luetkenii presence.The piscivorous fish species found in Cabiúnas Lagoon and observed in the macrophyte stands were Oligosarcus hepsetus and Hoplias malabaricus.Data for five piscivorous fishes (n=151 for all species) from Cabiúnas Lagoon showed that only O. hepsetus preyed upon Hyphessobrycon species (Rafael Leitão, pers.comm.).Oligosarcus hepsetus is a diurnal ambush predator, which suddenly attacks its prey from the bottom to the water surface (Sabino & Silva, 2004).It is possible that H. bifasciatus occupies the lagoon bottom in part to avoid predation by O. hepsetus, since occupying a position in the same stratum may allow it to perceive and escape from the predator.Since H. bifasciatus is more abundant than H. luetkenii (2.0 individuals/m 2 vs. 1.26 individuals/m 2 , from Sanchéz-Botero, 2005), the former may be excluding the latter from the potentially less-dangerous area.Sympatry between H. bifasciatus and H. luetkenii with other species of Oligosarcus is also reported in the Patos (Garcia & Vieira, 1997;2001) and Taim (Garcia et al., 2006) lagoons in southern Brazil, but no data on the use of space are available.
Overall, processes related to the spatial segregation between these species are still not clear, which provides impetus to search in detail for factors, such as predation, suspended particles distribution in the water column, and microhabitat characteristics, such as heterogeneity and complexity of macrophyte distribution, that may influence water-column segregation in this community.
We hypothesize that the observed pattern of vertical segregation was produced by a combination of predator avoidance and differential evolutionary adaptation, rather than by direct interspecies competition for space.
Fig. 1.Parque Nacional da Restinga de Jurubatiba (shaded area within the circle) in Rio de Janeiro State, southeastern Brazil.The satellite image shows Cabiúnas Lagoon, located in the southern part of the park.Asterisks indicate observation sites in the lagoon.