Emergence of Chironomidae ( Insecta : Diptera ) in a floodplain lake of the upper Paraná river , Mato Grosso do Sul State , Brazil

To investigate the emergence of Chironomidae in different habitats of a floodplain lake of the upper Paraná river floodplain, four collection points were established: marginal regions (one with numerous macrophytes species, other dominated by only Polygonum sp.), central region and linking channel. Adults were captured by surface emergence traps assembled every three months, from May 2001 to March 2002. The traps remained for a period of about 48 hours, obtaining quantitative data for richness and abundance. 944 adults distributed into three subfamilies and 40 taxa were captured. The taxa identified at the species level were: Goeldichironomus neopictus, G. petiolicola, G. maculatus, Tanytarsus ligulatus, Parachironomus atroari, P. guarani and P. cayapo. Higher abundances were observed for Polypedilum (Tripodura) sp.1 and Tanytarsus ligulatus. There was a considerable variation in the richness among the collection points, mainly on the marginal area, with 38 taxa. In the central region (five taxa) and in the linking channel, were registered the predominance of Aedokritus sp. The higher diversity and abundance of Chironomidae in the littoral area may be related to the presence of aquatic macrophytes that provide shelter and food, resulting in increased recruitment of new individuals in this region.


Introduction
Chironomidae is a group of aquatic insects frequently dominant among aquatic macroinvertebrates (CRANSTON, 2000).Few studies have evaluated the emergence of Chironomidae in aquatic communities because they are much diversified (MARCONDES; PINHO, 2005), exhibit multivoltine cycles (SONODA et al., 2005;STUR et al., 2006) and short life cycle, of only a few weeks (RAUNIO et al., 2007).
Chironomidae adult lifetime is usually very short, ranging from two to four days or several weeks, for reproduction, maturation and oviposition (CRANSTON, 2000).In the adult phase, individuals do not eat and some dominant species can exhibit a fast and highly synchronized, spatial and temporal emergence (VERBERK et al., 2008), with adults capable of flying immediately (SILVER; MCCAL, 2004).
The knowledge of the Chironomidae ecology in the Neotropical Region is primarily based on immature stages, often analyzed at the genus level, which consequently may limit the interpretation of population dynamics, habitat associations, and seasonal patterns of abundance (WILLIAMS; WILLIAMS, 1998).With regard to the identification at species level, most species recorded in the region was analyzed mainly by the morphology of adult forms, hindering the associations with immature forms and leading to a knowledge gap between larva and adult (TRIVINHO-STRIXINO, 2011).In this context, there is little information about the ecology of the different genera of adult Chironomidae, whose larvae are usually found associated with different habitats in a water body.
In this context, the present study investigated the spatial and seasonal patterns of emergent Chironomidae in different habitats (marginal region, central region and linking channel) of a Neotropical floodplain lake.We analyzed abundance, richness, diversity and dominance of adult Chironomidae.

Study area
The Ivinhema river is one of the large tributaries of the right bank of the Paraná river, surrounded by flooded areas and several marginal lakes (STEVAUX et al., 1997;SOUZA FILHO;STEVAUX, 2004).The Patos floodplain lake is a lentic water body, located at 22°43'12"S and 53°17'37"W, which remains permanently connected with the left bank of the Ivinhema river.
Four points of collection were established: PM1 -margin region, with predominance of Eichhornia.crassipes, Eichhornia.azurea, Salvinia auriculata and Polygonum sp.; PM2 -margin region next to the margin that separates the two water bodies, dominated by Polygonum sp., PRL -central region, and PM3 -linking channel between the lake and the river (Figure 1).
The Patos floodplain lake is characterized by similar limnological variables in all points (Table 1).
Adults of Chironomidae were captured every three months, from May 2001 to March 2002, with surface emergence traps (Figure 2).Each trap had a pyramidal form, whose base had 1.96 m 2 area, formed by four floating PVC tubes (10 cm of diameter) and it sustained nets with mesh of 0.1 mm On the top of the trap a collector containing 100 mL of formalin 4% was attached.Adults were collected 48 ± 2 hours after assembling the trap.The material collected was transferred to a funnel containing a support with a 0.2 mm mesh and all material was fixed in 70% alcohol.

Statistical analysis
The assemblage structure was analyzed using the Shannon-Wiener (H') diversity index (PIELOU, 1975), Margalef richness index, Evenness index (E) and dominance index of Kownacki (1971).The dominance index was subdivided into two groups: dominant (10  d  100) and subdominant (1  d  9.99) groups.Levene test was used for checking for the homogeneity of variance.The twoway ANOVA was used to test the differences between mean values of abundance in the habitats and months.
Procladius sp. was captured in three habitats while Cladopelma forcipis was registered only in the linking channel.
The taxonomic richness (Figure 3) and the abundance (Figure 4) were higher in the marginal regions, especially in October 2001, with 32 taxa and 352 individuals (SD±338 ind.) Both marginal regions showed the highest mean values of richness, evenness, and diversity indices (Simpon's and Shannon-Wiener's) (Table 3).

Discussion
From a developmental perspective, Chironomidae as well as many other aquatic insects are holometabolous, resulting in four distinct life stages: egg, larvae, pupa, and adult.The larval stage consists of an active benthic period, followed by a short pupal phase, also benthic, where the adult characteristics develop (OLIVER, 1971).After reaching maturity, the pupae begin the process of emergence where they move to the water surface, either through the water column or by crawling along vegetation.In the last stage of the life cycle, the insect undergoes both a metamorphosis to the adult form and a transition from the aquatic to the terrestrial environment (DAVIES, 1984).There is a short period of waiting at the water surface while the wings dry and open completely, after which the insect will emerge and fly away as an adult.
The high abundance of Chironomidae in the Patos floodplain lake was also observed for the larvae of this group by Higuti and Takeda (2002).The availability of Eichhornia azurea and E. crassipes on the marginal region could favor the colonization and development of larvae.
The emergence of Chironomidae over all collected months demonstrates that unlike studies developed in temperate or polar lakes (see SHERK; RAU, 1996), in the subtropical region the breeding activity is constant, with different species reproducing year round (TAKEDA et al., 2004;SIQUEIRA et al., 2008).
The high abundance in October indicates that this period is more favorable for the reproduction of Chironomidae, when temperatures and rainfall are beginning to increase.Associated with these conditions, the highest abundance in the marginal regions can be related with more shelter and resource in these areas, resulting in a high number of new recruitment.The highest abundance of Chironomidae adults in the Patos floodplain lake coincide with hotter and drier periods, probably related to the life cycle of each species and higher stability of the habitat.On the other hand, the results showed low abundance in emergence of adults in flood periods (March), mainly of Chironomus sp.3, Coelotanypus sp., Corynoneurini sp., Denopelopia cf.sp., Paranilothauma reissi and Polypedilum (Tripodura) sp.7.This result is probably related to the sediment washout and consequent reduction of organisms and parts of decaying macrophytes through advection (transfer of matter and organisms related to the horizontal movement of water masses) (SILVER; MCCAL, 2004).
These observations indicate that Chironomidae emergence is not a random event, but rather presents a relationship with environmental variables such as, temperature, water level, and oxygen concentration (NEUMANN; KRUGER, 1985;ARMITAGE, 1995).The emergence often occurs over a particular time of year depending on environmental conditions, however overall patterns are derived from the more specialized timing of each species.
Species of Chironomidae have short life cycle and the fecundity can also be related to certain periodicity (TRIVINHO-STRIXINO; STRIXINO, 2000STRIXINO, , 2005STRIXINO, , 2008;;SIQUEIRA et al., 2008).In this study, the emergence of some species such as Polypedilum (Tripodura) sp.1, Aedokritus sp. and Tanytarsus ligulatus has increased in the spring (October 2001).These species have adjusted to changes, thus presenting rapid life cycle and synchronism with environmental factors (SIQUEIRA et al., 2008).Species with rapid development and broad reproductive success were more abundant in water bodies with less predictable environmental conditions (VERBEK et al., 2008).
Tanytarsus larvae were found at high densities in many lakes of the alluvial plain of the upper Paraná river (HIGUTI; TAKEDA, 2002), which can be related to the high density of adults of T. ligulatus collected in this study.Many species of this genus living in lentic environments are associated with aquatic plants or living on sandy substrates (TRIVINHO-STRIXINO; SANSEVERINO, 2003).Higuti and Takeda (2002) and Higuti (2004) mentioned that larvae of Tanytarsus and Polypedilum (Tripodura) live on the surface of sediments with large amounts of debris and are found at higher densities in both shallow and marginal regions of sites from the upper Paraná river floodplain (HIGUTI, 2004).In this way, besides Polypedilum (Tripodura) sp.1 and Aedokritus sp., Tanytarsus ligulatus and Goeldichiromus maculatus species, respectively, dominant and subdominant in the habitats, they have adaptations to a multiplicity of environments, mainly during the dry season.
Environments such as linking channels can be important for the dispersion of organisms that comes from the main channel, especially for species presenting short life cycle, whose adults lay egg masses on the water surface (SILVER; MCCAL, 2004).
Despite of significant abundance and richness of Chironomidae, or possibly because of it, the group is often neglected in biological surveys (ARMITAGE, 1995, WILLIAMS;WILLIAMS, 1998;REYNOLDS;BENKE, 2006).The small size, superficial similarity, and high diversity make tempting to neglect the species level and treat Chironomidae at upper taxonomic levels.By doing so, researchers inhibit their ability to infer about ecological relationships, report changes in the community, and make adequate comparisons between systems.

Conclusion
This study brings an important contribution among the several researches on the diversity of the upper Paraná river floodplain.The knowledge of the whole life cycle is decisive for the maintenance and increase the diversity of aquatic insects, mainly the transition between the two developmental stages.Each species represents differences in the succession stages and transfer of energy and nutrients to external environments, providing food for higher trophic levels such as fish and birds.

Figure 1 .
Figure1.Map of the study area: PM1 -marginal region with macrophytes; PM2 -margin regional without macrophytes; PRC -Central region and PM3 -margin region of the linking channel.

Figure 3 .
Figure 3. Taxonomic richness in sampling months and habitats.

Figure 4 .
Figure 4. Individual's number in sampling months and habitats.

Table 1 .
Mean values and standard deviation of environmental variables in the collection points with emergence traps.Margin 1marginal region with macrophytes; Margin 2 -margin regional, with predominance of Polygonum sp.
Figure 2. Model of floating emergence trap for capturing adult insects.

Table 2 .
Mean abundance (standard deviation) and dominance index of Chironomidae adults in the habitats of the Patos Lake.

Table 3 .
Attributes of Chironomidae taxa in the different habitats of the Patos floodplain lake.H' = Shannon & Wiener's Diversity Index.