Passive zooplankton community in different environments of a neotropical floodplain

Zooplankton is able to respond promptly to environmental changes, producing resting forms in order to maintain populations when the conditions become unfavorable. The hatchling of the resting eggs was assessed in environments from the upper Paraná river floodplain, during the limnophase of 2008. We predicted that a higher production of these eggs and individuals’ hatchling are observed at isolated lakes, during dried period. Sediment samples were obtained with a corer sampler. The resting eggs were sorted and kept in filtered water from the same environment, in the laboratory. We recorded the occurrence of 378 resting eggs, of which 122 individuals hatched (70 cladocerans and 52 rotifers). The highest number of hatchlings was verified for the isolated lakes (84 individuals), as well the shorter time for hatchling (2 days). The hatchlings occurred mainly in September, when we registered the lowest hydrologic level of Paraná river (2.40 m). Grimaldina brazzai presented the longest time for hatchling, 44 days; and Brachionus dolabratus and B. falcatus, the shortest time, 2 days. This result suggests that the longer residence time of the water, which did not allow a renewal of food resources and limnological conditions of the environment, caused a higher stress in the zooplankton.


Introduction
Environments in the upper Paraná river floodplain show high diversity of zooplankton, stemming from the wide spatial heterogeneity and large fluctuations in water level caused by seasonal variations (LANSAC-TÔHA et al., 2004).
The colonization success of zooplankton populations in these environments is related to the strategies that allow the establishment and development of organisms in aquatic environments, as the production of dormant stages that enable the survival and maintenance of populations facing adverse environmental conditions (CRISPIM; WATANABE, 2000;FRYER, 1996;GILBERT, 1995;MAIA-BARBOSA et al., 2003).These stages are found in the sediment of aquatic environments and may remain viable for a long period of time (FRYER, 1996;MAIA-BARBOSA et al., 2003;RICCI, 2001).
Resting eggs from numerous species, produced at different times, compose an eggs bank that reflects the evolutionary history and environmental features of a given system (RICCI, 2001).Additionally, resting eggs enable the maintenance of genetic variability in the community (HAIRSTON; KEARNS, 1995), and contribute significantly for both temporal dynamics of active populations in the environment (CRISPIM et al., 2003;DE STACIO, 1990;HAIRSTON et al., 2000), and the dispersal of organisms (BILTON et. al., 2001;BRENDONCK;RIDDOCH, 1999;CÁCERES;SOLUK, 2002;JARNAGIN et al., 2000).
The factors that stimulate the production of resting stages may act distinctly on different species, and also among different populations within a same species.The intensity of production may also vary from one species to another (CACERES; TESSIER, 2004a and b;SCHRODER;GILBERT, 2004).
In this way, the present study aimed to evaluate the production and viability of resting eggs from zooplankton organisms, as well their time to hatchling, in eggs pool at connected and isolated lakes and backwaters from the upper Paraná river floodplain, during the periods of ebb and drought in 2008.We predicted that a greater number of eggs and hatchlings is verified in isolated lakes, during dry months.

Material and methods
We established different environments to this study: two backwaters (Pau Véio and Leopoldo Backwaters), three connected (Patos, Guaraná, and Garças Lakes) and four isolated lakes (Ventura, Fechada, Osmar and Genipapo Lakes), from the systems Paraná, Baia, and Ivinheima (Figure 1).Sediment samples were taken in different sampling points in the littoral and pelagic regions of the environments, according their size.In general, two samples were carried out in the environments during May, June, August, September and November 2008.There was not possible to sample in all environments during each months, mainly in August.Although major of them (7 environments) were sampled at the same time.The sediment samples were obtained using a corer sampler (194.5 cm 3 ), and we considered for analysis only the first five centimeters of the sediment.Samples were kept in dark flasks, and refrigerated (1-10 days) until laboratory analysis (MAIA-BARBOSA et al., 2003).
In order to obtain the resting eggs, the sediment samples were removed from refrigeration and kept under room temperature for 2 hours.Each sample was homogenized and 50 grams of sediment were diluted in a solution of sucrose and distilled water (MAIA-BARBOSA et al., 2003;ONBÉ, 1978).This solution was then centrifuged, at 3,600 rpm, for 5 minutes, and the supernatant was filtered through a 15 μm mesh net.
After this procedure, the material retained in the net was washed with distilled water and put into Petri dishes containing water from the same environment also filtered through 15 μm mesh net.The resting eggs were identified according to the literature and then they were examined daily, during 30 days, under a stereoscopic microscope (MAIA-BARBOSA et al., 2003) to verify the hatchling.After 30 days, unhatched eggs were examined every two days, and after three months (90 days) without hatchling, the hatchling experiments were finished.
Daily values of fluviometric levels of Paraná river were measured at Meteorological Station from the Agência Nacional de Energia Elétrica (ANEEL), located at the right bank of Paraná river, in Porto São José District.

Hydrological periods
Results from the hydrometric levels of Paraná river, responsible for the flood of floodplain environments, evidenced the occurrence of an ebb period in May (3.02 m) and June (2.86m), and a dry period in August (2.76 m), September (2.40 m) and November (2.74 m), since the level of 3.5 m is considered as reference for the floodplain overflow (SOUZA FILHO, 2009).

Composition of resting eggs from zooplankton organisms
The resting egg bank presented 20 taxa in the different environments, 12 cladocerans and 8 of rotifers, with prominence of the family Sididae (4 taxa) among the first group, and the family Brachionidae (6 taxa), for the second group (Table 1).
Table 1.Faunistic survey of zooplankton species present in the passive zooplankton community and the time to hatchling in the different environments of the upper Paraná river floodplain (PA = Patos lake, GA = Garças lake, FE = Fechada lake, VE = Ventura lake, OS = Osmar lake), in the period from May through November 2008.There were no hatchlings (x) in the backwater and Guaraná lake (connected lake).

Number of resting eggs and hatchlings
The time to hatchling of individuals from different species varied among the environments (Table 1).Individuals from the species Grimaldina brazzai presented the longest time, 44 days (one individual), from the eggs bank of Garças lake, in September.On the other hand, individuals of Brachionus dolabratus and B. falcatus presented the shortest time for hatchling, both with 2 days, from the eggs poll of the same lake, in May (Table 1).

Dynamic of zooplanktonic resting eggs
In the ebb period, we found a lower number of resting eggs (76 eggs) and hatchlings (3 hatchlings).On the other hand, a higher number of resting eggs was verified in the dry period (208 eggs) and, therefore a greater number of hatchlings (101 hatchlings), mainly of cladocerans (49 individuals) (Figure 3).

Discussion
The lower representativeness of rotifer resting eggs in the sediment of the lakes (156 resting eggs, 41.26%), when compared to cladocerans (222 resting eggs, 58.74%), is related to the greater resistance of this group to adverse environmental conditions.These results could be related to the opportunistic characteristics of rotifers, which allow their colonization in the most unstable environments (ALLAN, 1976), and this trait is often stressed in environments from floodplains (LANSAC-TÔHA et al., 2009;PAGGI;PAGGI, 2007).Moreover the resting eggs production has higher energetic cost than the parthenogenesis.In this way, rotifers, in general, produce just one egg (SANTANGELO, 2009).
The greater number of resting eggs in isolated lakes was related to the absence of connectivity with the river and the longer residence time (hydrodynamic instability) in this type of environment, which do not allow the constant renewal of water masses, and therefore representing a stress for the community in function of the degradation of optimal environmental conditions for the survival of active individuals (PALAZZO et al., 2008b).According to Simões (personal communication), these types of environments are more unstable than connected lakes, since they present a wide environmental variability, and changes in the environmental conditions could be surpass the limit of tolerance of some species.These relationships between zooplankton and environmental conditions in floodplain environments have also been pointed by Palazzo et al. (2008a) andSantangelo (2009).
In contrast, other studies showed that the hydrodynamic of connected lakes, indicated by the constant exchange of water with the river, does not favor the great production of zooplankton dormancy forms (PALAZZO et al., 2008b).
Regarding the time for hatchling, the longer time observed for one cladoceran species and the shorter, for two rotifer species, is certainly related to the life cycle of these organisms, since, according to Esteves (1998) the life cycle of microcrustaceans is quite longer than that of rotifers, which may last only one day.Palazzo et al. (2008b), in experiments performed with resting eggs sampled in one of the studied lakes, also observed that the cladoceran species did not hatch out all at once, however the time for hatchling did not ranged much, when compared with our study.(8 -12 days).Individuals of Ephemeropterus tridentatus, for example, lasted from 5 to 37 days to hatch out, from resting eggs present in the sediment from one same lake.Palazzo et al. (2008b) also showed that species exhibited 8 days to hatch out.
In relation to the lake where we sampled the resting eggs that presented the longer and the shorter time for hatchling (Garças lake), long term studies undertaken in this environment evidenced that the zooplankton was strongly influenced by environmental conditions, especially in function of environmental productivity (SIMÕES et al., 2009).
Analyzing the studied time scale, during the ebb period we found a lower number of resting eggs, and also lower hatchlings, whereas in the dry period we recorded a high number of resting forms and hatchlings.As above discussed, the dry period represent a strong stress for zooplankton organisms, since almost there is no exchange of nutrients, reduced primary production and colonized area, which could increase the competition for food and space.
The resting eggs sampled in September were those that presented a higher rate of hatchling, which is certainly related to the lower values of water temperature, dissolved oxygen, chlorophyll-a and pH, registered during the previous months in the different studied lakes.Thus, these environmental conditions may have induced the production of resting eggs.Studies developed by Palazzo et al. (2008b) showed a greater production of these resting stages in one of the studied lakes after a period with lower values of dissolved oxygen and lower phytoplankton production.The authors considered this latter as a stress factor for cladocerans, and concluded that a higher production of these eggs during this phase would guarantee the maintenance of populations of these microcrustaceans when the food resources were available again.Other studies also considered the food shortage as one of the main factor responsible for the diapause in these organisms (CRISPIM;WATANNABE, 2001;GILBERT, 1995;MAIA-BARBOSA et al., 2003).

Conclusion
The results support the predicted hypothesis, since, among the studied environments, the colonization process from resting eggs occurred more rapidly in the isolated lakes, during dry months.
Among the groups, cladoderans presented a higher production and hatchling of resting eggs, which are more sensitive to adverse environmental conditions, over time, nevertheless, rotifers tend to colonize the environments more quickly, presenting a shorter time for hatchling.

Figure 2 .
Figure 2. Number of resting eggs of zooplankton organisms and hatchlings, from May to November 2008 (TOTAL = total of resting eggs of zooplankton organisms, NC = number of eggs that not hatched, ECR = number of hatchlings of rotifers, and ECC = number of hatchlings of cladocerans).

Figure 3 .
Figure 3. Temporal variation in the number of resting eggs of zooplankton organisms found (A) and in the number of hatchlings from these eggs (B), in the period from May to November 2008.(symbol = mean of the sampling months and bar = standard error).