Oligochaetes (Annelida, Clitellata) in a neotropical stream: a mesohabitat approach

Oligoquetos (Annelida, Clitellata) em um córrego neotropical: uma abordagem do mesohabitat

Guilherme R. Gorni^I; Roberto da G. Alves^II

^IDepartamento de Ciências Biológicas e da Sáude, Centro Universitário de Araraquara - UNIARA, Rua Carlos Gomes 1338, Centro, 14801-340, Araraquara, SP, Brazil. ([e-mail])

^IIDepartamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Juiz de Fora - UFJF, Campus Universitário s/n°, Martelos, 36036-330, Juiz de Fora, MG, Brazil. ([e-mail])

ABSTRACT

This paper analyses the relationship among mesohabitat and aquatic oligochaete species in the Galharada Stream (Campos do Jordão State Park, state of São Paulo, Brazil). Between August 2005 and May 2006 a total of 192 samples were obtained in areas of four different mesohabitats: riffle leaf litter (RL), pool leaf litter (PL), pool sediment (PS) and interstitial sediment from rocky beds in riffle areas (IS). In the mesohabitats sampled, 2007 specimens were identified, belonging to two families (Naididae and Enchytraeidae). Among the oligochaetes identified Naididae was represented by six genera (Allonais, Chaetogaster, Nais, Pristina, Aulodrilus and Limnodrilus). Principal components analysis (PCA) revealed the first two axes explained 85.1% of the total variance of the data. Limnodrilus hoffmeisteri Claparede, 1862 and Aulodrilus limnobius Bretscher, 1899 were associated with the pool areas (PL and PS). Most species of genera Pristina and Nais demonstrated apparent affinity with the riffle mesohabitats. The Indicator Species Analysis (IndVal) revealed that Nais communis Piguet, 1906, Pristina leidyi Smith, 1896 and Pristina (Pristinella) jenkinae (Stephenson, 1931) are indicative of RL mesohabitat, while family Enchytraeidae was considered indicative of PL mesohabitat.

Keywords: Aquatic oligochaetes, community structure, mountain stream, Campos do Jordão State Park.

RESUMO

Este artigo analisou a relação entre mesohabitats e as espécies de oligoquetos aquáticos no Córrego Galharada (Parque Estadual de Campos do Jordão, Estado de São Paulo, Brasil). Entre agosto de 2005 e maio de 2006 um total de 192 amostras foram obtidas em quatro mesohabitats diferentes: folhiço em corredeiras (RL), folhiço em remanso (PL), sedimentos em remanso (PS) e sedimento intersticial de pedras em corredeiras (IS). Nos mesohabitats amostrados, foram identificados 2007 espécimes, pertencentes a duas famílias (Naididae e Enchytraeidae). Entre os oligoquetos identificados, Naididae foi representada por seis gêneros (Allonais, Chaetogaster, Nais, Pristina, Aulodrilus e Limnodrilus). A Análise de Componentes principais (ACP) revelou que os dois primeiros eixos explicaram 85,1% da variabilidade total dos dados. Limnodrilus hoffmeisteri Claparede, 1862 e Aulodrilus limnobius Bretscher, 1899 foram associadas às areas de remanso (PL e PS). A maioria das espécies dos gêneros Pristina e Nais demonstrou aparente afinidade com mesohábitats de corredeira. A análise de espécies indicadoras (IndVal) revelou que Nais communis Piguet, 1906, Pristina leidyi Smith, 1896 and Pristina (Pristinella) jenkinae (Stephenson, 1931) são indicadoras do mesohábitat RL, enquanto a família Enchytraeidae foi considerada indicadora do mesohábitat PL.

Palavras-chave: Oligoquetos aquáticos, estrutura da comunidade, córregos de montanha, Parque Estadual de Campos do Jordão.

Rivers and streams can be considered a network systems of areas with different size and environmental conditions (Clarke et al., 2008), where complex communities live. These ecosystems have a wide range of environmental conditions and the biotic communities have a variety of spatial scales, from microhabitats to entire landscapes and ecoregions (Heino et al., 2004).

Among the spatial scales, the "mesohabitat" is considered a useful unit in studies of natural ecosystems, because the physical factors (consequence of the micro-topography and hydrodynamics), food supply, reproduction and age of organisms and the biological interactions determine the structure of stream assemblages (Pardo & Armitage, 1997). According to Johnson et al. (2004), the variations of these factors explain changes in the spatial distribution of benthic macroinvertebrates, once these organisms relate dynamically with the changing habitat conditions (Beisel et al., 1998).

The community of benthic macroinvertebrates is an important indicator of great importance for understanding the structure and functioning of lotic ecosystems (Cummins, 1993), because this community is influenced by the processes that occur in these environments (Heino et al., 2003; Soldner et al., 2004). Studies of the spatial distribution of oligochaete species have shown that these invertebrates respond to the nature of the substrate and the water flow conditions (Stacey & Coates, 1996; Verdonschot, 1999, 2001; Alves et al., 2006; Schenková & Helešic, 2006, among others).

This contribution analyses the relationship among mesohabitat and aquatic oligochaetes species in the Galharada Stream, located in Campos do Jordão State Park in the state of São Paulo, Brazil. This paper has the null hypothesis that the nature of mesohabitat does not exert influence on aquatic oligochaetes species.

MATERIAL AND METHODS

Study area. The study was carried out in Campos do Jordão State Park (PECJ), located in the northern part of the municipality of Campos do Jordão, in the state of São Paulo (22°45'S, 45°39'W), covering an area of roughly 8,172 hectares, with altitude between 1,600 and 1,700 m, in the Mantiqueira mountain range (Seibert, 1975). The park's lotic environments are characterized as shallow, rich in riffles (or swifts) and pebbled substrate, with cool, clean and oxygenated water (Schroeder-Araujo et al., 1986). The samples were taken in Galharada Stream because its entire course is located within the park's limits.

Sampling and identification. Forty-eigth samples (12 for each mesohabitat) were taken for the quantitative sampling in each season from August 2005 to May 2006. The analysed months were August and November 2005, and February and May 2006, totalizing 192 samples. The organisms were collected using a Surber sampling device (McCafferty, 1981; Bicudo & Bicudo, 2004) with an area of 0.0362 m² and mesh of 0.25 mm. Four mesohabitat types were considered: riffle leaf litter (RL), pool leaf litter (PL), pool sediment (PS) and interstitial sediment in rocky riffle beds (IS) (Huamantinco & Nessimian, 2000). The material sampled was fixed in 10% formaldehyde and brought to the laboratory for examination under a stereoscopic microscope. The oligochaete species were identified and classified according to taxonomic criteria adopted by Brinkhurst & Jamieson (1971), Righi (1984), Brinkhurst & Marchese (1989), Collado & Schmelz (2000) and Erséus et al. (2008). The specimens identified were preserved in 70% alcohol and vouchers deposited in the Anelídeos collection of the Departmento de Zoologia of Universidade Federal de Juiz de Fora (UFJF) in Minas Gerais, Brazil.

Data analysis. The structure of the oligochaete assemblages was characterized by the abundance, richness of taxa and Shannon-Wiener diversity index (H'). The mesohabitats' richness was evaluated by rarefaction curves (Monte Carlo permutation method), using the lowest observed richness (320 organisms: IS mesohabitat). The procedures were performed using the program Ecosim 7 (Gotelli & Entsminger, 2004). To assess the effect of mesohabitats on the Shannon-Wiener diversity index was applied the One-Way ANOVA (α = 0.05).

The relation between the oligochaete species and the mesohabitats sampled was verified by Principal Components Analysis (PCA) after converting the data to logarithmic form [(log₁₀ (x+1)]. In this analysis, the juvenile Tubificidae specimens without hair chaetae were included in the species Limnodrilus hoffmeisteri Claparede, 1862. The Multivariate Statistical Package (MVSP - version 3.1) program was used to analyze the data.

The Indicator Species Analysis (IndVal) was performed to evaluate possible species typically associated with mesohabitats studied. This analysis was performed using the PC-ORD 5.15 (McCune & Mefford, 2006).

RESULTS

Taxonomic composition. After the identification, 2007, specimens were collected, representing two families: Naididae (15 species) and Enchytraeidae. The Naididae family was composed of six genera (Allonais, Chaetogaster, Nais, Pristina, Aulodrilus and Limnodrilus). The Enchytraeidae specimens were only identified to the family level. The oligochaetes identified and the respective occurrences in the mesohabitats sampled are listed in Tab. I.

The estimated richness did not differ between mesohabitats RL, IS and PL (12.7, 12.0, and 12.3 respectively), however was significantly lower in mesohabitat PS (7.8). According to One-Way ANOVA, the Shannon diversity index differ significantly between the sampled mesohabitats in the Galharada Stream (p = 0.000). The highest diversity index observed in RL mesohabitat (H' = 1.351), while the lowest diversity was observed in the PS mesohabitat (H' = 1.029) (Tab. II).

Principal component analysis (PCA). The first two PCA axes explained 85.14% of the faunistic data variation. Limnodrilus hoffmeisteri and Aulodrilus limnobius Bretscher, 1899 were associated with the pool areas (PL and PS) ordered on axis I (Fig. 1). The higher abundance of these species in relation to the others contributed to the low diversity in these mesohabitats. Pristina (Pristinella) notopora, Pristina (Pristinella) minuta (Stephenson, 1914), Pristina (Pristinella) sima (Marcus, 1944), Nais communis Piguet, 1906 and Nais variabilis Piguet, 1906 were negatively projected on the same axis, demonstrating greater affinity with the riffle mesohabitats. The first principal component synthesizes the effect of the water flow conditions, with the right side of the graph corresponding to the erosion zone (riffles) and the left side to the deposition zone (pools).

Axis II was composed positively of PS and IS mesohabitats, and negatively of the species Pristina proboscidea Beddard, 1895, Pristina leidyi Smith, 1896, Pristina (Pristinella) jenkinae (Stephenson, 1931), Pristina (Pristinella) longidentata (Harman, 1965) and Chaetogaster diastrophus (Gruithuisen, 1828), which were abundant in the PL and RL mesohabitats. The second principal component synthesizes the effect of the type of substrate in the mesohabitats, with the upper part corresponding to the mesohabitats with mineral substrate (IS and PS) and the lower part to those with organic substrate (PL and RL).

Indicator Species Analysis (IndVal). The IndVal revealed four taxa indicators of mesohabitats RL and PL, and no taxa indicator of mesohabitats IS and PS (details on Tab. III).

DISCUSSION

The variation diversity index may reflect the hydraulic conditions and type of substrate in the composition of oligochaete assemblages in the mesohabitats sampled. According to Pardo & Armitage (1997), the types of substrate and flow pattern result in a mosaic distribution of species in mesohabitats, each inhabited by particular assemblages of indicator species. In general, majority of the oligochaetes considered as indicators prefer specific habitats and the occurrence of these habitats depends on a complex interaction between different substrate types and water flow patterns (Verdonschot, 2001).

According to Beisel et al. (1998), the species richness increases with the heterogeneity of the habitat and the total abundance rises with the food availability, while the diversity of species tend to increase with the stability of the substrate. Our results demonstrate most varied communities mainly in habitats with greater apparent structural complexity (accumulation of leaves, corresponding availability of food in the form of organic litter).

Disregarding the effect of abundance, Mathooko & Otieno (2002) reported that increased richness of invertebrate species can be explained by the micro and macrostructures that define the textural complexity of the plant detritus, such as the presence of furrows, holes and undulations. Taniguchi & Tokeshi (2004) stated that the habitat complexity is important because of its influence on the food supply and places of refuge against fast water flow and agile predators.

According to Dangles et al. (2001), leaf accumulations play another important role, namely the retention of organic particles suspended in the water column, influencing the richness and abundance of the invertebrates that colonize these habitats. The organic matter content, even in low concentrations, is very important since it permits colonization by fungi and bacteria, on which oligochaetes feed (Alves & Strixino, 2000). In contrast, the rocky substrates, because they are more stable, influence the composition of the communities differently, by providing more hiding places for invertebrates in search of refuge and food (Effenberger et al., 2006).

The Principal Components Analysis (PCA) showed that the aspects that most influenced the structure and composition of the oligochaete fauna were differences in water flow (pools versus riffles), making the substrate secondary, though still important. Martínez-Ansemil & Collado (1996) and Pardo & Armitage (1997) both considered that current speed and substrate stability are the main factors to explain the spatial distribution of oligochaete species.

The result of the PCA analysis suggest that L. hoffmeisteri was associated with still habitats with fine sediment (PS), corroborating the information reported by Verdonschot (1989), Dumnicka & Kukula (1990), Marchese & Drago (1999), Timm et al. (2001) and Alves et al. (2006). Similarly, the tubificid Aulodrilus limnobius was present mainly in still-water habitats with large amounts of allochtonous organic material (leaves and twigs). On the other hand, Montanholi-Martins & Takeda (2001) reported A. limnobius in the erosion zone of the Ivinhema River (state of Paraná, Brazil), inhabiting coarse sediment, while Nijboer et al. (2004) stated that this species is typical of running water. These reports along with our findings show that this species can occur in habitats with or without current and in substrates with different physical characteristics. According to Dumnicka & Kukula (1990), the tubificids are most numerous in places with weak or no current, where organic matter accumulates. Pristina (Pristinella) notopora was associated with running-water habitats in pebbled or sandy beds. However, Stacey & Coates (1996) reported this species as being associated with muddy substrates slightly enriched with organic matter.

The Indicator Species Analysis showed that Nais communis, Pristina leidyi and Pristina (Pristinella) jenkinae are indicator of environments with running water and accumulation of allochtonous organic material. Dumnicka (1976, 1982) also reported the species of Nais in environments with similar physical conditions to the stream we studied. Nevertheless, Dumnicka & Kukula (1990) and Lencioni et al. (2004) reported that these species prefer standing water. Pristina leidyi was reported by Learner et al. (1978) on pebbles, and P. (P.) jenkinae was reported to be associated with muddy and sandy substrates and submersed vegetation (Stacey & Coates, 1996). The family Enchytraeidae was pointed as an indicator of habitat with standing water and accumulation of sandy sediment. The enchytraeids are essentially terrestrial oligochaetes but many species have marked aquatic tendencies. Healey & Bolger (1984) recorded the tendency of some species inhabit soils which were submerged or frequently flooded. According Johnson & Ladle (1989) most Enchytraeidae adopt a "generalist" ecological strategy, being able to inhabit a wide range of environments (can cope with variations in hydrological conditions, temperature and salinity).

In general, the results reveal a complex relationship between the oligochaete fauna and nature of the mesohabitats, supporting the information of Schenková & Helešic (2006) that the majority of oligochaete species have wide ecological amplitude and habitat preferences. Martínez-Ansemil & Collado (1996) have also concluded that aquatic oligochaetes of different geographic regions show different preferences for type of substrate and current speed, a quality that considerably expands the variation of their distribution.

Acknowledgments. To Professor Tarmo Timm for their valuable suggestions on the manuscript. To Marcia R. Spies and whole team coordinated by Professor Cláudio Gilberto Froehlich (USP Ribeirão Preto) for field assistance. To (FAPESP) BIOTA/ Program for logistics support, and to CAPES for financial support.

Recebido em 18 de novembro 2011.

Aceito em 26 de março de 2012.

ISSN 0073-4721

• Alves, R. G. & Strixino, G. 2000. Distribuição espacial de Oligochaeta do sedimento de uma lagoa marginal do rio Mogi-Guaçu-SP. Iheringia, Série Zoologia 88:173-180.
• Alves, R. G.; Marchese, M. R. & Escarpinati, S. C. 2006. Oligochaeta (Annelida: Clitelata) in lotic environments in the state of São Paulo (Brazil). Iheringia, Série Zoologia 96(4):431-435.
• Beisel, J. N.; Usseglio-Polatera, P.; Thomas, S. & Moreteau, J. C. 1998. Stream community structure in relation to spatial variation: the influence of mesohabitat characteristics. Hydrobiologia 389:73-88.
• Bicudo, M. & Bicudo, D. C. 2004. Amostragem em Limnologia São Carlos, RiMa. 371p.
• Brinkhurst, R. O. & Jamieson, B. G. M. 1971. Aquatic Oligochaeta of the World Edinburgh, Oliver & Boyd. 860p.
• Brinkhurst, R. O. & Marchese, M. R. 1989. Guia para la indentificacion de Oligoquetos aquáticos continentales de Sud y Centroamerica Santa Fé, Asociación de Ciencias Naturales del Litoral. 270p.
• Clarke, A.; Nally, R. M.; Bond, N. & Lake, P. S. 2008. Macroinvertebrate diversity in headwater streams: a review. Freshwater Biology 53:1707-1721.
• Collado, R. & Schmelz, R. M. 2000. Pristina silvicola and Pristina terrena spp. nov., two new soil-dwelling species of Naididae (Oligochaeta, Annelida) from the tropical rain forest near Manaus, Brazil, with comments on the genus Pristinella Journal of Zoology 251:509-516.
• Cummins, K. W. 1993. Invertebrates. In: Calow P. & Petts, G. E. eds. The Rivers Handbook - Hydrological and Ecological Principles Oxford, Blackwell Science. p. 234-250.
• Dangles, O.; Guerold, F. & Usseglio-Polatera, P. 2001. Role of transported particulate organic matter in the macroinvertebrate colonization of litter bags in streams. Freshwater Biology 46:575-586.
• Dumnicka, E. 1976. Oligochaetes (Oligochaeta) of some streams of the High Tatra Mts and of the River Balka Tatrzańska. Acta Hydrobiologica 18(3):305-315.
• _____. 1982. Stream ecosystems in mountain grassland (West Carpathians); 9. Oligochaeta. Acta Hydrobiologica 24(4):391-398.
• Dumnicka, E. & Kukula, K. 1990. The communities of oligolchaetes of the Wolosatka and Terebowiec streams the Bieszczady National Park, southeastern Poland. Acta Hydrobiologica 30(3/4):423-435.
• Effenberger, M.; Sailer, G.; Townsend, C. R. & Matthaei, C. D. 2006. Local disturbance history and habitat parameters influence the microdistribution of stream invertebrates. Freshwater Biology 51:312-332.
• Erséus, C.; Wetzel, M. J. & Gustavsson, L. 2008. ICZN rules - a farewell to Tubificidae (Annelida, Clitellata). Zootaxa 1744:66-68.
• Gotelli, N. J. & Entsminger, G. L. 2004. EcoSim: Null Models Software for Ecology Version 7.0 Acquired Intelligence Inc. & Kesey-Bear. Available at: <http://garyentsminger.com/ecosim/index.htm.>. Accessed on: 25.07.2011.
• Healey, B. & Bolger, T. 1984. The occurrence of species of semi-aquatic Enchytraeidae in Ireland. Hydrobiologia 115:159-170.
• Heino, J.; Louhi, P. & Muotka, T. 2004. Identifying the scales of variability in stream macroinvertebrate abundance, functional composition and assemblage structure. Freshwater Biology 49:1230-1239.
• Heino, J.; Muotka, T. & Paavola, R. 2003. Determinants of macroinvertebrate diversity in headwater streams: regional and local influences. Journal of Animal Ecology 72:425-343.
• Huamantinco, A. A. & Nessimian, J. L. 2000. Variation and life estrategies of the Trichoptera (Insecta) larvae community in a first order tributary of the Paquequer River, Southeastern Brazil. Revista Brasileira de Zoologia 60(1):73-82.
• Johnson, P. & Ladle, M. 1989. The Enchytraeidae (Oligochaeta) of streams of Southern England. Annales de Limnologie 25(2):121-129.
• Johnson, R. K.; Goedkoop, W. & Sandin, L. 2004. Spatial scale and ecological relationships between the macroinvertebrate communities of stony habitats of streams and lakes. Freshwater Biology 49:1179-1194.
• Learner, M. A.; Lochhead, G. & Hughes, B. D. 1978. A review of the biology of the British Naididae (Oligochaeta) with emphasis on the lotic environment. Freshwater Biology 8:357-375.
• Lencioni, V.; Dumnicka, E. & Maiolini, B. 2004. The oligochaete fauna in high mountain streams (Trentino, NE Italy): ecological and taxonomical remarks. Studi trentini di scienze naturali, Acta biologica 81:167-176.
• Marchese, M. & Drago, I. E. 1999. Use of benthic macroinvertebrates as organic pollution indicators in lotic environments of Paraná River drainage basin. Polish Archives of Hydrobiology 46(3-4):233-255.
• Martínez-Ansemil, E. & Collado, R. 1996. Distribution patterns of aquatic oligochaetes inhabiting watercourses in the Northwestern Iberian Peninsula. Hydrobiologia 334:73-83.
• Mathooko, J. M. & Otieno, C. O. 2002. Does surface textural complexity of woody debris in lotic ecosystems influence their colonization by aquatic invertebrates? Hydrobiologia 489:11-20.
• McCafferty, W. P. 1981. Aquatic Entomology: The fisherman's and ecologist's illustrated guide to insects and their relatives Boston, Science Books International. 448p.
• McCune, B. & Mefford, M. J. 2006. PC-ORD - Multivariate analysis of ecological data Version 5.10. Oregon, MjM Software.
• Montanholi-Martins, M. C. & Takeda, A. M. 2001. Spacial and temporal variations of oligochaetes of Ivinhema River and Patos Lake in the Upper Paraná River Basin, Brazil. Hydrobiologia 463:197-205.
• Nijboer, R. C.; Wetzel, M. J. & Verdonschot , P. F. M. 2004. Diversity and distribution of Tubificidae, Naididae, and Lumbriculidae (Annelida: Oligochaeta) in the Netherlands: An evaluation of twenty years of monitoring data. Hydrobiologia 520:127-141.
• Pardo, I. & Armitage, P. D. 1997. Species assemblages as descriptors of mesohabitats. Hydrobiologia 344:111-128.
• Righi, G. 1984. Manual de identificação de invertebrados límnicos do Brasil Brasília, CNPq/Coordenação Editorial. 48p.
• Schenková, J. & Helešic, J. 2006. Habitat preferences of aquatic Oligochaeta (Annelida) in the Rokytná River, Czech Republic - a small highland stream. Hydrobiologia 564:117-126.
• Schroeder-Araujo, L. T.; Stempniewski, H. L.; Cipolli, M. N.; Santos, L. E.; Santo-Paulo, M. & Correa-Cremonesi, W. 1986. Estudo Limnológico e Climatológico da Região do Parque Estadal de Campos do Jordão, SP, com vistas ao povoamento com truta Arco-Íris, Salmo irideus Gibbons. Boletim do Instituto de Pesca 13(2):63-76.
• Seibert, P. 1975. Plano de manejo do Parque Estadual de Campos do Jordão. Boletim Técnico do Instituto Florestal de São Paulo 19:1-153.
• Soldner, M.; Stephen, I.; Ramos, I.; Angus, R., Wells, N. C.; Grosso, A. & Crane, M. 2004. Relationship between macroinvertebrate fauna and environmental variables in small streams of the Dominican Republic. Water Research 38:863-874.
• Stacey, D. F. & Coates, K. A. 1996. Oligochaetes (Naididae, Tubificidae, Opistocystidae, Enchytraeidae, Sparganophilidae and Alluroididae) of Guyana. Hydrobiologia 334:17-29.
• Taniguchi, H. & Tokeshi, M. 2004. Effect of habitat complexity on benthic assemblages in a variable environment. Freshwater Biology 49:1164-1178.
• Timm, T.; Seire, A. & Pall, P. 2001. Half a century of oligochaete research in Estonian running waters. Hydrobiologia 463:223-234.
• Verdonschot, P. F .M. 1989. The role of oligochaetes in management of waters. Hydrobiologia 180:213-217.
• _____. 1999. Micro-distribution of oligochaetes in a soft-bottomed lowland stream (Elsbeek; Netherlands). Hydrobiologia 406:149-163.
• _____. 2001. Hydrology and substrates: determinants of oligochaete distribution in lowland streams (The Netherlands). Hydrobiologia 463:249-262.

Oligochaetes (Annelida, Clitellata) in a neotropical stream: a mesohabitat approach

Oligoquetos (Annelida, Clitellata) em um córrego neotropical: uma abordagem do mesohabitat

Publication Dates

• Publication in this collection
  15 May 2012
• Date of issue
  Mar 2012

History

• Received
  18 Nov 2011
• Accepted
  26 Mar 2012