Plankton rotifers from a tropical lake: differences in distribution and migration patterns in two mixing events, with similar abiotic conditions

Rotíferos planctónicos de un lago tropical: diferencias en la distribución y migración entre dos eventos de mezcla con condiciones abióticas similares

Sandra A. Zanatta¹, Roberto Torres-Orozco B.¹, J. Alejandro Zavala-Hurtado² and Marco A. Pérez-Hernández²

¹ Departamentos de Hidrobiología Universidad Autónoma Metropolitana - Iztapalapa. Apartado Postal 55-535, C.P. 09340, México, D.F. E-mail rotor@xanum.uam.mx

Recibido: 05 de diciembre de 2005
Aceptado: 29 de agosto de 2006

Abstract

Vertical distribution of plankton rotifers is not random. Although the causes of this behavior are still under debate, it has been suggested, mainly from the study of stratified environments, that abiotic parameters play an important role in determining the presence and position of a species in the water column. We compared the composition and vertical distribution of planktonic rotifers in a tropical monomictic lake in Mexico during the mixing period of two years in which abiotic conditions were similar. We recorded 28 rotifer species. Total average densities ranged from 238±39 ind l^-1 to 517±97 ind l^-1. The similarity of rotifer assemblages between the two compared dates was 46.4%. Our Results showed that temperature and dissolved oxygen in the upper 13 meters and pH upper 8 meters, respectively, were homogeneous in the two dates. Nevertheless, the rotifer assemblages showed important differences in: a) the absolute population densities, b) the dominance ranking of species in the community, c) the preferential position of a specific species in the water column, d) the relationship between such preference and the studied abiotic factors and, e) the types and amplitudes of species' migrations. Given the resemblance of the abiotic factors in the analyzed years, we suggest that changes in rotifers distribution and abundance would involve biological factors, such as food availability, competition and predation. .

Key words: abiotic factors, diel vertical migration, distribution and abundance, freshwater zooplankton, Mexico.

Resumen

Palabras clave: Factores abióticos, migración vertical diaria, distribución y abundancia, zooplankton dulceacuícola, México.

Introduction

Most vertical distribution patterns of zooplankton species result from a daily active migration process. Nowadays, it is known that although migration can be produced by a multiplicity of factors, this behavior would be optimized by natural selection. This would be reflected in each population's fitness and in the entire dynamics of lake ecosystems (Lampert & Sommer, 1997).

Given the ecological importance of plankton rotifers and the scarcity of information on their communities in Mexican freshwaters, this study aims to describe some community parameters (composition, density, frequency and dominance), as well as the vertical distribution patterns and migration dynamics of the most important rotifer species in a Mexican lake.

Since rotifer communities comprise dynamic interacting populations, species assemblages may differ both temporally and spatially. Although it is recognized that species distribution of the planktonic rotifers is not random (Ruttner-Kolisko, 1974; Armengol et al., 1998), the causes of these patterns are still under debate (Huntley, 1985). In several studies that have explored the relationship of plankton rotifers with abiotic, environmental parameters (e.g., temperature, pH, Secchi disk transparency and dissolved oxygen) it has been suggested that these parameters act as key factors in determining the composition (May, 1983; Matveeva, 1986; Berzins & Pejler, 1987, 1989a, 1989b; Mikschi, 1989) and vertical distribution (Ruttner-Kolisko, 1980; Armengol et al., 1993; Armengol & Miracle, 1999; Esparcia et al., 2001) of rotifer assemblages.

To explore the above-mentioned idea, we also analyzed the community structure and vertical distribution of the plankton rotifers of a lake in two different periods with very similar abiotic conditions. To make this inter-date comparison we chose two dates within turnover periods of the lake for two important reasons. First, because most abiotic parameters are more homogeneous throughout the water column during mixing (Wetzel, 2001; Kalff, 2002) and, second, because the majority of the studies that have found close relationships between abiotic factors and rotifer distribution patterns have been performed in stratified environments, which could lead us to understandable but questionable cause-effect assumptions.

In this study, we compared the patterns of abundance and vertical distribution of plankton rotifers of a tropical lake, derived from the analysis of two diel cycles carried out in different years. In addition, we explored the relationships among these patterns and some abiotic factors. Our study was performed under the hypothesis that if factors like temperature, dissolved oxygen and pH, are actually controlling rotifer populations behavior; when these factors do not differ significantly between two sampling times, the structure and behavior of the rotifer assemblages should not differ as well.

Laguna Escondida is a warm tropical, monomictic lake located in South-eastern Mexico (18° 35' N; 95° 06' W, 130 m asl), in the middle of the Los Tuxtlas Region, at the Mexican State of Veracruz. The climate is warm and humid, with mean annual temperature of 27°C, and although it rains throughout the year, it is possible to distinguish a rainy season, from June to February, and a dry period from March to May (Torres-Orozco et al., 1994). The lake is surrounded by the remnants of a tropical rain forest; it has an area of 18.23 ha and a maximum depth of 32.5 m, with annual narrow water-level variations. It circulates regularly between January and March and remains stratified the rest of the year. During mixing, the water column becomes homothermic at 20-21 °C or differs only by 1°C from surface to the bottom. In contrast, during the stratification period, a vertical temperature gradient of 6-7°C is established. Even under homothermic conditions, both the depth of the lake and constant input of allochthonous organic matter allow a clinogradic profile of dissolved oxygen to persist; thus, hypolimnetic anoxia is common during the hottest and rainiest part of the year, from August to October (Torres-Orozco et al., 1996).

We have been sampling with some regularity the plankton of this lake since 1993; so, to make the comparison that led us to test our working hypothesis, we chose the two available dates with the higher resemblance in vertical distribution of the water column abiotic factors during the mixing period of the lake. These dates were January 26-27, 1996 and February 2-3, 2003.

In both dates, a 24-hour sampling program was carried out at the center of the lake at a depth of 17.5 m, and samples were collected at three-hr intervals, between 15:00 hrs in the first day and 12:00 hrs the following day. The sampling depths were 0.25, 1.0, 1.5, 2.0, 3.0, 5.0, 8.0, 12.0 and 16.0 m in 1996, and 0.25, 1.5, 3.0, 5.0, 8.0, 12.0 and 17.0 m in 2003. Water samples were taken with a 3.0 l van Dorn bottle for the determination of temperature (digital thermometer Cole Parmer 90201-10, -40 to 120°C ±0.2 °C), pH (pH meter Corning M103) and dissolved oxygen (Winkler method). Secchi disk transparency was also measured. Plankton samples were collected with a Schindler-Patalas type trap with 30.85 l of capacity, provided with a 54-µm mesh net, and preserved in 4% buffered formaldehide.

Subsamples of previously concentrated plankton samples were placed in a 1.0 ml Sedgwick-Rafter plankton-counting cell (50 x 20 x 1 mm) and rotifers were counted with an optic microscope at ×100 magnification. The whole volume of three cells was counted in all cases.

A Mann-Whitney non-parametric test was used in order to evaluate the inter-annual differences in the mean values of temperature, dissolved oxygen and pH at different depths in the water column. Olmstead and Tukey association diagrams (Steel & Torrie, 1988) were used to identify the dominant species in the rotifer community, based on the frequency and abundance of each species. We analyzed individually each 24-hr cycle.

To assess the statistical differences in depth distribution of the dominant rotifer populations along the diel cycle (i.e. if the individuals of each species congregate in certain depths at different hours of the day), a log-likelihood ratio (G) test on contingency tables (Sokal & Rohlf, 1995) was performed.

The patterns of diel vertical migration were established from the shifts in the mean residence depth (MRD) of each dominant population. This was estimated by

MRD = Σ(n_i ^× d_i) / Σn_i

where n_i is the number of individuals at depth i, and d_i is the depth of the i-th sample (Armengol & Miracle, 2000).

Results

The water temperature and DO in the upper 13 m during 1996 and 2003 did not differ significantly (t-test); this was true also for pH in the upper 8 m. Below these depths all these parameters differed significantly (p < 0.004, p< 0.005, and p< 0.004, respectively; Fig. 1). The main difference between both years was related to the location of oxygen drops, which varied from 8.4 to 6.0 mg O₂ l^-1 (between 4.0 and 8.0 m) in 1996 and from 5.5 to 3.5 mg O₂ l^-1 (between 12 and 13 m) in 2003. The depth of Secchi disk transparency was 1.2 m in both years.

Rotifers constituted >70% of total zooplankton species during both years; 26 and 25 rotifer species were detected in 1996 and 2003, respectively. We recorded a total of 28 species (23 common to both dates) from 15 genera and 11 families. Brachionidae, with four genera and eight species, was the best represented family, and the most diverse genus was Lecane (Table 1).

In 1996, 11 species were the most frequent and abundant; in order of importance were Keratella tropica, Trichocerca pusilla, Polyarthra vulgaris, Ascomorpha saltans, Keratella americana, Brachionus calyciflorus, Collotheca sp., Ascomorpha ecaudis, Hexarthra mira, Trichocerca similis and Synchaeta pectinata. On the other hand, in 2003, only eight species were dominant: B. calyciflorus, A. ecaudis, A. saltans, S. pectinata, K. tropica, P. vulgaris, K. americana and T. pusilla. Thus, seven of the 11 dominant species in 1996 maintained their dominance also in 2003 (Fig. 2). The rest of the community included Anuraeopsis fissa, Asplanchna brigthwelli, Brachionus quadridentatus, Lecane closterocerca, Trichocerca dixon-nuttalli, and other 12 species with very low densities and frequencies (Fig. 2).

The average rotifer densities varied significantly (p < 0.001): from 238.09±39.21 ind l^-1 in 1996 to 517.50±97.39 ind l^-1 in 2003. Although species composition was similar in both years, important differences were observed in their dominance ranking (Fig. 2). In 1996, Keratella tropica was the most abundant and frequent species. With an average density of 104.50±165.09 ind l^-1, it contributed 42.9 % to the total density, whereas B. calyciflorus only contributed 3.6%. In 2003, B. calyciflorus became more abundant (324.70±379.73 ind l^-1, on the average), comprising 63% of the total rotifer density, with K. tropica contributing only 4.6% to the total. The Morisita similarity index (Krebs, 1989) showed a resemblance value among the two years of 46.4%.

A G test showed that the vertical distributions of most of these species along the diel cycle were different (p<0.025) because of a real aggregation of species populations in certain depths as a function of the time of the day (Fig. 3). Exceptions to this were K. americana, T. pusilla and P. vulgaris, in 2003, whose vertical gradient in the water column showed to be independent of the time of the day (p> 0.1). The observed changes in the vertical distribution of the dominant species through the diel cycle suggest the existence of migratory behavior in most cases. This is more clearly depicted in the MRD plots (Fig. 4).

Hexarthra mira had the highest migration amplitude, 6.42 m, in 1996 and Polyarthra vulgaris the lowest, 1.72 m, in 2003. Except for K. americana and H. mira, migration amplitudes were similar for all species in both cycles (Table 2).

Discussion

Most of the studies that relate the distribution patterns of plankton rotifers with abiotic factors have been carried out in stratified environments (e. gr. Armengol et al., 1998; Armengol & Miracle, 1999; Baião & Boavida, 2000; Esparcia et al., 2001). Under these hydrological conditions, close correlations between such factors and rotifer populations have been recognized. In the above mentioned studies it is concluded that in correspondence to water stratification there are rotifer assemblages characteristic of each main strata. Under this scenario, it is clear that the position of a species within a stratum would show a strong correlation with the prevailing abiotic factors. Nevertheless, the existence of such correlations does not necessarily imply a cause-effect relationship because very different factors could actually be involved in the control of rotifer populations.

Temperature and oxygen are among the most important environmental factors acknowledged to explain the space-time fluctuations of rotifer populations (Bogaert & Dumont, 1989; Mikschi, 1989). However, in addition to direct effects of temperature and oxygen, the effects of these variables on rotifer fluctuations could be mediated via other biotic and abiotic factors.

Although seven years elapsed between the two sampling dates, when comparing the vertical distribution of temperature, oxygen and pH no significant differences were observed in the uppermost 10 meters of the water column. Secchi disk transparency was also the same in both periods. Given that our Results show that most of the dominant rotifer populations had their abundance peaks and vertical movements within this part of the water column, the observed differences in rotifer vertical distributions could hardly be attributed to the influence of these factors.

In both years, the lake was practically homothermic and differences of only 1 to 1.3 °C were detected in the 18-m water column. Additionally, oxygen levels were always far from anoxia and compatible with the physiological requirements of the rotifer species. The oxygen content in 2003, generally lower and with a more pronounced drop than that in 1996, could be attributed to increased input of allochthonous organic matter due to a heavy rain that occurred the day before the sampling date. Under such conditions, the organic matter can deplete oxygen concentrations quickly, but at the same time, it constitutes an important food source for certain rotifer populations. Therefore, probably, rotifer species in such situations did not respond to changes in oxygen levels but to food availability.

Since the absence of thermal stratification reduces the influence of abiotic processes on spatial distribution, the degree of vertical aggregation in homothermic environments may be better explained by biotic factors such as food availability (Johnsen & Jakobsen, 1987; Bini et al., 2001). Furthermore, this factor could also partially explain differences in composition and abundance of rotifer assemblages (May, 1983; Baião & Boavida, 2000). The replacement of K. tropica by B. calyciflorus as the most dominant species in 2003 seems to agree with this idea. It is known that B. calyciflorus has the highest rate of population increase among metazoans (r= 2 per day, under laboratory conditions; Benett & Boraas, 1989), and also that this rate is strongly dependent on a high food supply (Sarma et al., 1996, 1999). Thus, the increase in density of this and other abundant species in 2003 may be due to higher food availability.

Furthermore, it is known that the structure of zooplankton communities is strongly regulated by biotic interactions, such as predation and competition (DeMott & Kerfoot, 1982; DeMott, 1989; Leibold, 1990; José De Paggi, 1995; Lampert and Sommer, 1997). Moreover, habitat segregation would be an important mechanism that allows the coexistence of potential competitors (Schoener, 1974; Leibold, 1990, 1991). In Laguna Escondida A. ecaudis and S. pectinata, that are of similar size and share the same feeding strategy (both are raptors that suck out the cytoplasm of their preys: Nogrady et al., 1993; Ruttner-Kolisko, 1974), showed DVM patterns suggesting they would avoid interspecific competition by means of space-time segregation (Fig. 4).

The rotifers of Laguna Escondida share the water column with crustacean zooplankters like the copepods Thermocyclops inversus Kiefer, 1936, and Tropocyclops prasinus (Fischer, 1860), and the cladocerans Moina micrura Kurz, 1874, and Daphnia parvula Fordice,1901, which also migrate (Torres-Orozco & Estrada-Hernández, 1997). Therefore, interference or exploitative competition between rotifers and some of these species would be expected. Regarding predation, the lake is inhabited by important populations of poecillid fishes of the genera Xiphophorus, Poecilia, Heterandria and Priapella, as well as some species of Astyanax and Cichlasoma (Torres-Orozco & Estrada-Hernández, 1997) that, indeed, can prey on rotifers. Thus, the presence of these predators could also play a significant role in the rotifers' population dynamics.

The three basic types of migration, i.e., nocturnal or "normal" migration, twilight migration, and reversed migration (Hutchinson, 1967), were recognized in the diel vertical movements of dominant rotifers (Fig. 4; Table 2). Nevertheless, some species showed important differences in their migration patterns. Thus, Ascomorpha ecaudis changed its migratory movements from a normal type in 1996 to a reversed type in 2003. Although less clearly, A. saltans showed also a shift but in this case from a reversed type in 1996 to the normal type in 2003. Even though the migration patterns of some species were not easily assignable to a certain type, in most cases they appeared to be of the reversed type. In Synchaeta pectinata, the reversed type of migration was clear and consistent in both years (Fig. 4).

In the preferential position (i. e. MRD's) of rotifers along the water column, three different species categories could be recognized: a) species with relatively small vertical movements in the upper water column (e.g. B. calyciflorus, P. vulgaris and T. pusilla), b) species with noticeable movements between the middle and upper portions of the water column (e.g.: Ascomorpha ecaudis, A. saltans and S. pectinata) and, c) species with variable vertical displacements associated to deeper waters (e.g.: H. mira and K. americana, mainly in 2003). However, our Results show that each species' habitat is a dynamic feature that may change with time. Examples are H. mira and K. americana, whose preferential positions moved to higher depths in 2003, or of T. pusilla and K. tropica that, although remaining in the same category, changed significantly their MRD in the two studied years. It is noteworthy that in contrast with Armengol and Miracle (2000), who found H. mira in the well-oxygenated surface waters of a Spanish lake, we in 2003 found this species inhabiting water layers close to the bottom, where oxygen levels were the lowest recorded (3.2 ± 0.57 mg l^-1).

The migration amplitudes observed for some species also differed from those reported in other lakes. Armengol and Miracle (2000), for example, found relatively low values for A. saltans, H. mira and S. pectinata (2.0, 2.5 and 1.3 m, respectively), whereas we observed notably higher values for these species (see Table 2). In addition, for S. pectinata they reported a normal migration type while, in our study, it was a clearly reversed one.

In summary, when comparing rotifer assemblages from different years with similar abiotic conditions, important differences became discernible in: a) the absolute population densities, b) the species dominance ranking, c) the preferential position of specific species in the water column, d) the relationship between such preference and the abiotic factors and, e) the types and amplitudes of their migrations. So, our working hypothesis was not supported by our data. The behavioral plasticity observed herein could be better explained with arguments of biological nature, but there are required further research efforts to unveil the actual role of biological interactions in the structuring of rotifer communities.

Acknowledgements

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