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Hyporheic invertebrate assemblages at reach scale in a Neotropical stream in Brazil

Assembleia de invertebrados em grande escala em um riacho Neotropical no Brasil

Abstract

In the Neotropical Region, information concerning hyporheic communities is virtually non-existent. We carried out a sampling survey in the hyporheic zone of the Tijuca River, in the Tijuca National Park, located in the urban area of the city of Rio de Janeiro. Biological samples from the hyporheic zone were collected in three different stream reaches, in June 2012. The main objectives were: 1) to describe the structure of invertebrate assemblages in the hyporheic zone of a neotropical stream; 2) to apply a reach-scale approach in order to investigate spatial patterns of the hyporheic assemblages in relation to hydrology, depth and microhabitat typology. A total of 1460 individuals were collected and identified in 31 taxa belonging to Nematoda, Annelida, Crustacea, Hydrachnidia and Insecta. The class Insecta dominated the upper layer of the hyporheic zone. Copepods were the most abundant taxon among crustaceans and occurred mostly in the upwelling areas of the reaches. The results of this study represent one of the few contributions so far about hyporheic invertebrate assemblages of the Neotropical Region.

Keywords:
hyporheic zone; Neotropical Region; stygobites; stygophiles; stygoxenes

Resumo

Na Região Neotropical, informações sobre comunidades de invertebrados de zona hiporréica são praticamente inexistentes. Foi realizado um levantamento da zona hyporréica do Rio Tijuca, no Parque Nacional da Tijuca, localizado na área urbana da cidade do Rio de Janeiro. As amostras biológicas da zona hiporréica foram coletadas em três diferentes trechos do riacho, em junho de 2012. Os principais objetivos foram: 1) descrever a estrutura das assembléias de invertebrados na zona hiporréica de um riacho neotropical, 2) aplicar uma abordagem de grande escala de trecho de riacho com finalidade de investigar os padrões espaciais das assembléias hiporréicas em relação à hidrologia, profundidade e tipologia de microhabitat. Um total de 31 táxons foram identificados pertencentes à Nematoda, Annelida, Crustacea, Hydrachnidia e Insecta. A classe Insecta dominou a camada superior da zona hiporréica. Copépoda foi o taxon mais abundante entre os crustáceos e ocorreu principalmente nas áreas de resurgência de água. Os resultados deste estudo representam uma das poucas contribuições até o momento sobre assembléias de invertebrados de zona hiporréica em região Neotropical.

Palavras-chave:
zona hiporréica; Região Neotropical; estigóbios; estigófilos; estigóxenos

1 Introduction

The hyporheic zone (HZ) is the interstitial active ecotone between the surface stream and ground water, where exchanges of water, biota, nutrients and organic matter occur (Orghidan, 1959Orghidan, T., 1959. Ein neuer Lebensraum des unterirdischen Wasser: der hyporheische Biotop. Archiv für Hydrobiologie, vol. 55, pp. 392-414.; Schwoerbel, 1967Schwoerbel, J., 1967. Das hyporheische Interstitial als Grenzbiotop zwischen oberirdischem und subterranem Ökosystem und seine Bedeutung für die Primär-Evolution von Kleinsthöhlenbewohnern. Archiv für Hydrobiologie, vol. 33, no. 6, pp. 1-62.; Boulton et al., 1998Boulton, A.J., Findlay, S., Marmonier, P., Stanley, E.H. and Valett, M., 1998. The functional significance of the hyporheic zone in streams and rivers. Annual Review of Ecology and Systematics, vol. 29, no. 1, pp. 59-81. http://dx.doi.org/10.1146/annurev.ecolsys.29.1.59.
http://dx.doi.org/10.1146/annurev.ecolsy...
; Bencala, 2000Bencala, K.E., 2000. Hyporheic zone hydrological processes. Hydrological Processes, vol. 14, no. 15, pp. 2797-2798. http://dx.doi.org/10.1002/1099-1085(20001030)14:15<2797::AID-HYP402>3.0.CO;2-6.
http://dx.doi.org/10.1002/1099-1085(2000...
, 2005Bencala, K.E., 2005. Hyporheic exchange flows. In: M.G. ANDERSON and J.J. MCDONNELL, eds. Encyclopedia of hydrological sciences. New Jersey: John Wiley and Sons, vol. 3, chap. 113, pp. 1733-1740.). At reach scale, in opposition to surface water, the hyporheic water flow is laminar but not unidirectional. A maze of flow paths of different lengths, directions and velocities occurs, generated by reach-scale geomorphological features such as discontinuities in slope and depth of riffle-pool sequences, channel shape and streambed structure (Boulton et al., 1998Boulton, A.J., Findlay, S., Marmonier, P., Stanley, E.H. and Valett, M., 1998. The functional significance of the hyporheic zone in streams and rivers. Annual Review of Ecology and Systematics, vol. 29, no. 1, pp. 59-81. http://dx.doi.org/10.1146/annurev.ecolsys.29.1.59.
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). Along a single riffle-pool alternation, surface water enters the HZ in a downwelling area at the riffle head (or at the end of a pool), and hyporheic water returns to stream surface in an upwelling area at the riffle tail (or at the head of a pool) after travelling in the HZ (Thibodeaux and Boyle, 1987Thibodeaux, L.J. and Boyle, J.D., 1987. Bedform-generated convective transport in bottom sediment. Nature, vol. 325, no. 6102, pp. 341-343. http://dx.doi.org/10.1038/325341a0.
http://dx.doi.org/10.1038/325341a0...
; Boulton et al., 1998Boulton, A.J., Findlay, S., Marmonier, P., Stanley, E.H. and Valett, M., 1998. The functional significance of the hyporheic zone in streams and rivers. Annual Review of Ecology and Systematics, vol. 29, no. 1, pp. 59-81. http://dx.doi.org/10.1146/annurev.ecolsys.29.1.59.
http://dx.doi.org/10.1146/annurev.ecolsy...
and references herein), in a process known as hyporheic exchange (Harvey and Wagner, 2000Harvey, J.W. and Wagner, B.J., 2000. Quantifying hydrologic interactions between streams and their subsurface hyporheic zones. In: J.B. JONES and P.J. MULHOLLAND, eds. Streams and ground waters. San Diego: Academic Press. pp. 3-44.). Laterally, water flow enters and leaves the HZ proceeding from stream banks and vice versa, according to geomorphological features (Jones Junior and Holmes, 1996Jones JUNIOR, J.B. and Holmes, R.M., 1996. Surface subsurface interactions in stream ecosystems. Trends in Ecology & Evolution, vol. 11, no. 6, pp. 239-242. http://dx.doi.org/10.1016/0169-5347(96)10013-6. PMid:21237825.
http://dx.doi.org/10.1016/0169-5347(96)1...
). Hyporheic flow patterns regulate physical and chemical conditions in the HZ, determining microbial activity and occurrence of hyporheic fauna too (Franken et al., 2001Franken, R.J.M., Storey, R.G. and Williams, D.D., 2001. Biological, chemical and physical characteristics of downwelling and upwelling zones in the hyporheic zone of a north-temperate stream. Hydrobiologia, vol. 444, no. 1/3, pp. 183-195. http://dx.doi.org/10.1023/A:1017598005228.
http://dx.doi.org/10.1023/A:101759800522...
). According to the degree of adaptation to subsurface habitats, hyporheic species can be attributed to one of three diverse ecological categories: stygoxenes, that have no affinities with the underground environment and occur in it only accidentally; stygophiles, that actively explore the resources of the HZ, at least in part of their life cycle; stygobites, that are specialized to live in underground and complete their lifecycle in subsurface waters only (Gibert et al., 1994Gibert, J., STANFORD, J.A., DOLE-OLIVIER, M.-J. and WARD, J.W., 1994. Basic attributes of groundwater ecosystems and prospects for research. In: J. GIBERT, D.L. DANIELOPOL and J.A. STANFORD, eds. Groundwater ecology. San Diego: Academic Press, pp. 7-40.). The stygophiles can be further subdivided into three categories: the occasional hyporheic fauna, predominantly consisting of benthic insects, mainly larvae, that may spend part of their lifetime in this environment under specific circumstances like simulids; amphibites, namely species with lifecycle related to both surface and subsurface environments, mostly represented by insects like chironomids and some species of ephemeropterans; permanent hyporheos, namely species that may be present during all life stages either in benthic habitats and in ground water, like nematodes, oligochaetes, copepods, ostracods, cladocerans, tartigrades and mites (Gibert et al., 1994Gibert, J., STANFORD, J.A., DOLE-OLIVIER, M.-J. and WARD, J.W., 1994. Basic attributes of groundwater ecosystems and prospects for research. In: J. GIBERT, D.L. DANIELOPOL and J.A. STANFORD, eds. Groundwater ecology. San Diego: Academic Press, pp. 7-40.). Hyporheic invertebrate communities typically exhibit high spatial and temporal heterogeneity due to several biotic and abiotic factors, at all scales (Boulton et al., 1998Boulton, A.J., Findlay, S., Marmonier, P., Stanley, E.H. and Valett, M., 1998. The functional significance of the hyporheic zone in streams and rivers. Annual Review of Ecology and Systematics, vol. 29, no. 1, pp. 59-81. http://dx.doi.org/10.1146/annurev.ecolsys.29.1.59.
http://dx.doi.org/10.1146/annurev.ecolsy...
; Brunke and Gonser, 1997Brunke, M. and Gonser, T., 1997. The ecological significance of exchange processes between rivers and groundwater. Freshwater Biology, vol. 37, no. 1, pp. 1-33. http://dx.doi.org/10.1046/j.1365-2427.1997.00143.x.
http://dx.doi.org/10.1046/j.1365-2427.19...
). At reach scale, the structure of hyporheic assemblages may be strongly influenced by the nature of substratum which affects the ability of organisms to move, settle, gather food, and find shelter (Olsen et al., 2001Olsen, D.A., Townsend, C.R. and Matthaei, C.D., 2001. Influence of reach geomorphology on hyporheic communities in a gravel ‐ bed stream. New Zealand Journal of Marine and Freshwater Research, vol. 35, no. 1, pp. 181-190. http://dx.doi.org/10.1080/00288330.2001.9516988.
http://dx.doi.org/10.1080/00288330.2001....
; Omesová and Helešic, 2007Omesová, M. and Helešic, J., 2007. Vertical Distribution of Invertebrates in Bed Sediments of a Gravel Stream in the Czech Republic. International Review of Hydrobiology, vol. 92, no. 4-5, pp. 480-490. http://dx.doi.org/10.1002/iroh.200610990.
http://dx.doi.org/10.1002/iroh.200610990...
; Omesová et al., 2008Omesová, M., Horsák, M. and Helešic, J., 2008. Nested patterns in hyporheic meta-communities : the role of body morphology and penetrability of sediment. Naturwissenschaften, vol. 95, no. 10, pp. 917-926. http://dx.doi.org/10.1007/s00114-008-0399-3. PMid:18542903.
http://dx.doi.org/10.1007/s00114-008-039...
). The occurrence of riffle-pool sequences has been proved to be a major determining factor of the patterns of hyporheic assemblages. In particular, more oxygenated downwelling zones are often dominated by stygoxenes and stygophiles, whereas stygobites may prevail in the upwelling areas which are less rich in oxygen (Marmonier et al., 1992Marmonier, P., Dole-Olivier, M.J. and Creuze Des Châtelliers, M., 1992. Spatial distribution of interstitial assemblages in the floodplain of the Rhône River. Regulated Rivers: Research and Management, vol. 7, no. 1, pp. 75-82. http://dx.doi.org/10.1002/rrr.3450070110.
http://dx.doi.org/10.1002/rrr.3450070110...
; Brooks and Boulton, 1991Brooks, S.S. and Boulton, A.J., 1991. Recolonization dynamics of benthic macroinvertebrates after artificial and natural disturbances in an Australian temporary stream. Australian Journal of Marine and Freshwater Research, vol. 42, no. 3, pp. 295-308. http://dx.doi.org/10.1071/MF9910295.
http://dx.doi.org/10.1071/MF9910295...
). The insect larvae are generally confined to the upper layers of the HZ; however, some species penetrate deeper and can be an important component of the hyphoreic fauna, called hyporheos (Stanford and Ward, 1988Stanford, J.Á. and Ward, J.V., 1988. The hyporheic habitat of river ecosystem. Nature, vol. 335, no. 6185, pp. 64-66. http://dx.doi.org/10.1038/335064a0.
http://dx.doi.org/10.1038/335064a0...
; Brooks and Boulton, 1991Brooks, S.S. and Boulton, A.J., 1991. Recolonization dynamics of benthic macroinvertebrates after artificial and natural disturbances in an Australian temporary stream. Australian Journal of Marine and Freshwater Research, vol. 42, no. 3, pp. 295-308. http://dx.doi.org/10.1071/MF9910295.
http://dx.doi.org/10.1071/MF9910295...
; Lencioni, 2004Lencioni, V., 2004. Survival strategies of freshwater insects in cold environments. Journal of Limnology, vol. 63, no. 1s, pp. 45-55. http://dx.doi.org/10.4081/jlimnol.2004.s1.45.
http://dx.doi.org/10.4081/jlimnol.2004.s...
; Fenoglio et al., 2006Fenoglio, S., Bo, T. and Bosi, G., 2006. Deep interstitial habitat as a refuge for Agabus paludosus (fabricius) (Coleoptera: Dytiscidae) during summer droughts. Coleopterists Bulletin, vol. 60, no. 1, pp. 37-41. http://dx.doi.org/10.1649/842.1.
http://dx.doi.org/10.1649/842.1...
; Lencioni et al., 2008Lencioni, V., Marziali, L. and Rossaro, B., 2008. Hyporheic chironomids in alpine streams. Boletim do Museu Municipal do Funchal, vol. 13, pp. 127-132.). The benthic invertebrates may use the HZ in order to escape competition or predation (Schwoerbel, 1967Schwoerbel, J., 1967. Das hyporheische Interstitial als Grenzbiotop zwischen oberirdischem und subterranem Ökosystem und seine Bedeutung für die Primär-Evolution von Kleinsthöhlenbewohnern. Archiv für Hydrobiologie, vol. 33, no. 6, pp. 1-62.; Williams and Hynes, 1974Williams, D.D. and Hynes, H.B.N., 1974. The occurrence of benthos deep in the substratum of a stream. Freshwater Biology, vol. 4, no. 3, pp. 233-256. http://dx.doi.org/10.1111/j.1365-2427.1974.tb00094.x.
http://dx.doi.org/10.1111/j.1365-2427.19...
). Moreover, they actively exploit it as a nursery and shelter from the disturbance induced by the movement of the substrate and the variations of the environmental conditions due to seasonal flooding and droughts (Schwoerbel, 1967Schwoerbel, J., 1967. Das hyporheische Interstitial als Grenzbiotop zwischen oberirdischem und subterranem Ökosystem und seine Bedeutung für die Primär-Evolution von Kleinsthöhlenbewohnern. Archiv für Hydrobiologie, vol. 33, no. 6, pp. 1-62.; Williams and Hynes, 1974Williams, D.D. and Hynes, H.B.N., 1974. The occurrence of benthos deep in the substratum of a stream. Freshwater Biology, vol. 4, no. 3, pp. 233-256. http://dx.doi.org/10.1111/j.1365-2427.1974.tb00094.x.
http://dx.doi.org/10.1111/j.1365-2427.19...
; Dole-Olivier et al., 1997Dole-OlivIer, M.J., Marmonier, P. and Beffy, J.L., 1997. Response of invertebrate to lotic disturbance: is the hyporheic zone a patchy refugium? Freshwater Biology, vol. 37, no. 2, pp. 257-276. http://dx.doi.org/10.1046/j.1365-2427.1997.00140.x.
http://dx.doi.org/10.1046/j.1365-2427.19...
; Lencioni, 2004Lencioni, V., 2004. Survival strategies of freshwater insects in cold environments. Journal of Limnology, vol. 63, no. 1s, pp. 45-55. http://dx.doi.org/10.4081/jlimnol.2004.s1.45.
http://dx.doi.org/10.4081/jlimnol.2004.s...
; Lencioni et al., 2008Lencioni, V., Marziali, L. and Rossaro, B., 2008. Hyporheic chironomids in alpine streams. Boletim do Museu Municipal do Funchal, vol. 13, pp. 127-132.; James and Suren, 2009James, A.B.W. and Suren, A.M., 2009. The response of invertebrates to a gradient of flow reduction: an instream channel study in a New Zealand lowland river. Freshwater Biology, vol. 54, no. 11, pp. 2225-2242. http://dx.doi.org/10.1111/j.1365-2427.2009.02254.x.
http://dx.doi.org/10.1111/j.1365-2427.20...
; Stubbington, 2012Stubbington, R., 2012. The hyporheic zone as an invertebrate refuge: a review of variability in space, time, taxa and behavior. Marine & Freshwater Research, vol. 63, no. 4, pp. 293-311. http://dx.doi.org/10.1071/MF11196.
http://dx.doi.org/10.1071/MF11196...
). Other groups perform vertical migrations: Tricladida, Nematoda, Annelida, Crustacea, Acari (Hynes, 1975Hynes, J.D., 1975. Annual cycles of macroinvertebrates of a river in southern Ghana. Freshwater Biology, vol. 5, no. 1, pp. 71-83. http://dx.doi.org/10.1111/j.1365-2427.1975.tb00122.x.
http://dx.doi.org/10.1111/j.1365-2427.19...
; Godbout and Hynes, 1982Godbout, L. and Hynes, H.B.N., 1982. The three dimensional distribution of the fauna in a single riffle in a stream in Ontario. Hydrobiologia, vol. 97, no. 1, pp. 87-96. http://dx.doi.org/10.1007/BF00014962.
http://dx.doi.org/10.1007/BF00014962...
; Olsen and Townsend, 2003Olsen, D.A. and Townsend, C.R., 2003. Hyporheic community composition in a gravel-bed stream: influence of vertical hydrological exchange, sediment structure and physiochemistry. Freshwater Biology, vol. 48, no. 8, pp. 1363-1378. http://dx.doi.org/10.1046/j.1365-2427.2003.01097.x.
http://dx.doi.org/10.1046/j.1365-2427.20...
).

In Brazil, as elsewhere in the Neotropical Region, information concerning hyporheic communities are scarce. This study was aimed at enhancing the bulk of information on this matter. The main objectives were: 1) to describe the structure of invertebrate assemblages in the HZ of a neotropical stream in the Rio de Janeiro State, Brazil; 2) to apply a reach-scale approach in order to investigate the spatial patterns of the hyporheic assemblages in relation to hydrology, depth and microhabitat typology.

2 Methods

2.1 Study area

The Tijuca National Park is entirely located in the urban area of the city of Rio de Janeiro (Figure 1), between S 22° 55’– S 23° 00’ and W 43° 11’ – W 43° 19’, with a forested area of approximately 32 km2. The vegetation is typical of the Atlantic forest. From a historical point of view, this area was extensively deforested for coffee cultivation in the XVII and XIX centuries and it was subsequently reforested using native and some exotic species (Mattos et al., 1976Mattos, C.C.L.V., Mattos, M.D.L.V. and Laroche, R.C., 1976. Aspectos do clima e da flora do Parque Nacional do Tijuca. Brasil Flor, vol. 7, pp. 3-12.). The secondary forest is the typical tropical rainforest that occurs along the Brazilian coast. The climate is humid tropical with average annual temperature between 20 °C and 25 °C. The annual rainfall rate is higher than 1,500 mm. The rainy season occurs between November and February (rainfalls > 250 mm/month), and the dry season from June to September (rainfalls < 100 mm/month). The geological substratum predominantly consists in granite (Brasil, 1987BRASIL. Ministério das Minas e Energia, 1987. Projeto Radambrasil: levantamento de recursos naturais. Rio de Janeiro: Ministério das Minas e Energia. vol. 32, 780 p.).

Figure 1
Study area, stream reaches and sampling sites in the Tijuca River, Tijuca National Park, Rio de Janeiro city, State of Rio de Janeiro, Brazil. P letters indicate the stream reaches.

Biological samples from the HZ were collected in three stream reaches (PI, PII and PIII), in June 2012, respectively located in the first, second and third Strahler order (sensuStrahler, 1957Strahler, A.N., 1957. Quantitative analysis of watershed geomorphology. T. American Geophysical Union, vol. 38, no. 6, pp. 913-920. http://dx.doi.org/10.1029/TR038i006p00913.
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) in the Tijuca River (Figure 1). The three reaches are quite different. PI is the steepest; boulders represent 80% of the riverbed with a 20% of sand. The PII is the least steep and sand represents 60% of the riverbed, with regular riffle–pool alternations. In the PIII reach, boulders represent 60% of the riverbed; riffle-pool sequences are less regular and separated by long areas of deposition of fine sediments. Habitat assessment was done with visual-based habitat assessment (Barbour et al., 1999Barbour, M.T., Gerritsen, J., Snyder, B.D. and Stribling, J.B., 1999. Rapid bioassessment protocols for use in streams and Wadeable Rivers: periphyton, benthic macroinvertebrates and fish. 2nd ed. Washington, D.C.: EPA. 197 p.).

2.2 Sampling methodology

At each reach, PVC mini-piezometers, 2.5 cm in diameter and 150 cm in length, were used to collect samples from the HZ at three different depths: 10, 25 and 45 cm. The design of traditional piezometers (see Lee and Cherry, 1978Lee, D.R. and Cherry, J.A., 1978. A field exercise on groundwater flow using seepage meters and mini-piezometers. Journal of Geological Education, vol. 27, pp. 6-10.; Valett, 1993Valett, H.M., 1993. Surface-hyporheic interactions in a Sonoran Desert stream: hydrologic exchange and diel periodicity. Hydrobiologia, vol. 259, no. 3, pp. 133-144. http://dx.doi.org/10.1007/BF00006593.
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;) was modified reducing the height of perforated bands to 5 cm, in order to allow a stratified sampling (Figure 2). The diameter of the slots was 5 mm. For each depth, five mini-piezometers were positioned in five different habitats: riffle heads, riffle tails, lateral side of pools, areas of sand accumulation, namely bars and curves. Riffle heads represented downwelling habitats. Riffle tails and lateral sides of curves were considered zones of longitudinal and lateral upwelling, respectively. Sand accumulation areas were taken into account as zones of equilibrium between up- and downwelling. In the PIII reach, at 45 cm in depth, no water was found. Consequently, 40 mini-piezometers were located, overall. In order to guarantee the independence of samples, the mini-piezometers were positioned at least 1.5 meters from each other (Boulton et al., 2007Boulton, A.J., Marmonier, P. and Sarriquet, P.-E.X., 2007. Hyporheic invertebrate community composition in streams of varying salinity in south-western Australia: diversity peaks at intermediate thresholds. River Research and Applications, vol. 23, no. 6, pp. 579-594. http://dx.doi.org/10.1002/rra.989.
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). Samples were collected using a modified Bou-Rouch pump (Vigna Taglianti et al., 1969Vigna Taglianti, A., Cottarelli, V. and Argano, R., 1969. Messa a punto di metodiche per la raccolta della fauna interstiziale e freatica. Archivio Botanico e Biogeografico Italiano, vol. 45, no. 14, pp. 375-380.). For each mini-piezometer, a sample of five liters of water and sediments was taken (Boulton et al., 2004Boulton, A.J., Dole-Olivier, M.-J. and Marmonier, P., 2004. Effects of sample volume and taxonomic resolution on assessment of hyporheic assemblage composition sampled using a Bou-Rouch pump. Archiv für Hydrobiologie, vol. 159, no. 3, pp. 327-355. http://dx.doi.org/10.1127/0003-9136/2004/0159-0327.
http://dx.doi.org/10.1127/0003-9136/2004...
; EA, 2009ENVIRONMENT AGENCY – EA, 2009. The hyporheic handbook: a handbook on the groundwater-surface water interface and hyporheic zone for environment managers. Bristol: Environment Agency. Science Report, SC050070.; Kibichii et al., 2009Kibichii, S., Baars, J. and Kelly-Quinn, M., 2009. Optimising sample volume and replicates using the Bou-Rouch method for the rapid assessment of hyporheic fauna. Marine & Freshwater Research, vol. 60, no. 1, pp. 83-96. http://dx.doi.org/10.1071/MF08172.
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). In order to separate fine sediments, POM and invertebrates, the samples were elutriated in the field and filtered by a net with a mesh of 68 µm and preserved in a 75% alcohol solution. In laboratory, the samples were treated with rose bengal for 48 hours (Brown, 1975Brown, H.D., 1975. A counterstaining technique for use in sorting benthic sample? Limnology and Oceanography, vol. 19, pp. 152-154.), before sorting under a stereomicroscope. The specimens were counted and removed using tweezers and glass pipettes. Individuals were identified at the lowest taxonomic level allowed by a magnification of 40 x: genus or family for insect´s larvae, order for crustaceans with exception of family Parastenocaridae and phylum for anelidians and nematans (Appendix 1 Appendix 1 Sampling sites and taxa abundances (number of individuals). Site codes include information about: Strahler order (I: first Strahler order; II: second Strahler order; III: third Strahler order); sampling depth: numbers indicates cm of depth beneath the streambed (10, 25 and 45); habitats type (A: riffle head; B: riffle tail; C: lateral side of pools; D1: bars: D2: curves). CHIR: Chiromidae; DIXI: Dixidae; oCERA: other Ceratopogonidae; CULI: Culicoides; LEPT: Leptoconops; MARU: Maruina; TIPU: Tipulidae; SIMU: Simulidae; PSYC: Psychodidae; dLARV: Elmidae Larva d; NEOE: Neoelmis; DYTI: Dytiscidae; PERL: Perlidae; niEPHE: non identified Ephemeroptera; BAET: Baetidae; LEPT: Leptophlebiidae; OECE: Oecetis; NECT: Nectopsiche; HELI: Helicopsiche; GRUM: Grumicha; MARI: Marlia; CYRN: Cyrnellus; HYDR: Hydroptilidae; COLL: Collembola; CYCL: Cyclopoida; PARA: Parastenocarididae; Ahar: Harpacticoida morphotype "a"; OSTR: Ostracoda; CHYD: Chidoridae; BATH: Bathynellacea; HYIA: Hydrachnidia; NEMA: Nematoda; ANN: Annelida. ID Site CHIR DIXI oCERA CULI LEPT MARU TIPU SIMU PSYC dLARV NEOE DYTI PERL niEPHE BAET LEPT OECE NECT HELI GRUM MARI CYRN HYDR COLL CYCL PARA Ahar OSTR CHYD BATH HYIA NEMA ANNE 26 I10A 5 0 0 5 0 0 3 0 0 0 2 0 0 0 0 0 0 0 0 0 0 2 0 0 1 0 4 1 0 0 4 0 4 27 I10B 12 0 0 17 1 1 0 0 1 0 0 0 0 2 0 0 1 0 0 0 0 0 0 1 1 0 14 1 0 0 14 0 1 28 I10C 20 0 0 3 0 0 1 0 0 0 0 0 0 0 2 0 0 0 0 2 0 0 0 0 0 0 9 4 1 0 5 2 8 29 I10D1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 1 2 1 30 I10D2 7 0 0 2 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 3 0 0 31 125IA 3 0 0 2 0 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 1 0 0 4 1 1 32 125B 3 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 2 3 5 33 I25C 4 0 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 10 1 4 0 1 0 4 1 3 34 125D1 7 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 1 0 0 0 1 0 0 2 11 35 I25D2 2 0 0 1 0 0 2 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 2 36 I45A 5 0 0 2 0 0 1 3 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 2 4 7 0 0 7 9 2 37 I45B 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 10 1 1 1 0 0 3 0 2 38 I45C 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 5 0 0 39 I45D1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 3 0 0 40 I45D2 1 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 3 0 0 0 0 1 1 1 II10A 6 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 1 0 2 0 0 9 4 2 2 II10B 15 0 0 14 0 0 3 0 0 0 0 0 1 2 0 0 0 0 0 0 0 0 0 0 6 9 9 12 14 0 7 17 61 3 II10C 21 0 0 0 0 0 1 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 25 7 5 3 13 0 9 4 4 4 II10D1 27 0 0 3 0 0 3 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 27 4 5 0 2 0 7 1 20 5 II10D2 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 6 II25A 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 1 1 7 II25B 42 0 6 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 2 7 7 1 0 3 0 6 6 0 8 II25C 30 0 2 0 0 0 0 0 0 0 1 0 0 2 0 0 0 0 0 0 1 0 0 0 1 29 1 0 3 0 13 1 0 9 II25D1 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 1 1 0 10 II25D2 3 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 1 0 11 II45A 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 14 2 1 3 12 II45B 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 1 0 13 II45C 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 6 0 8 3 5 1 1 3 5 14 II45D1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 9 0 1 0 0 1 2 0 1 15 II45D2 7 1 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 1 0 3 0 1 0 1 1 0 16 III10A 17 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 2 2 4 2 11 0 9 14 1 17 III10B 21 0 0 0 0 0 0 0 0 0 1 0 0 0 3 0 0 0 0 0 0 0 0 0 8 1 6 7 13 0 14 5 4 18 III10C 15 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 2 1 0 0 0 0 0 0 2 19 III10D1 24 0 0 3 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 1 0 1 1 0 0 7 2 1 20 III10D2 36 0 0 2 2 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 2 3 4 2 0 12 18 10 21 III25A 7 0 0 4 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 2 2 0 0 0 5 5 4 22 III25B 7 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 2 23 III25C 5 0 0 1 0 0 0 0 0 0 3 0 0 0 0 0 0 0 1 0 0 0 0 0 1 4 0 2 7 0 2 1 0 24 III25D1 4 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 1 0 0 0 6 0 0 25 III25D2 3 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 4 0 1 1 4 0 2 3 2 ).

Figure 2
Mini-piezometers and position of perforated bands at different sampling depths.

2.3 Statistical analyses

We analyzed the biological data of the HZ of Tijuca River at each sampling site for abundances (individuals per site) and taxa diversity considering Strahler order of stream reaches, depth and microhabitat typology as factors influencing biological patterns. Taxonomic richness and Shannon’s and Simpons’ indices were used to asses taxa diversity. Shapiro-Wilk test was used to test for normal distribution of biological data Since the data were not normally distributed, a non-parametric ANOVA was applied. Kruskal-Wallis tests, followed by post-hoc t-tests corrected through Bonferroni method, was carried out in order to detect differences in abundances and taxa composition, separately. The test was applied only to those variables with homogeneous variances, after applying a non-parametric Levene test. Multifactorial analysis was additionally used to identify the taxa that mostly contributed to site discrimination. Biological patterns were explored by a Principal Coordinate Analysis (PCoA) on log-transformed abundances of all taxa. All statistical analyses were performed by the R software, version 2.15.0 (R Development Core Team, 2013R DEVELOPMENT CORE TEAM, 2013. R: A language and environment for statistical computing. Version 2.15.0 [software]. Vienna: R Foundation for Statistical Computing.).

4 Results

A list of hyporheic taxa, identified during the survey, and their relative abundances is given in the Appendix 1 Appendix 1 Sampling sites and taxa abundances (number of individuals). Site codes include information about: Strahler order (I: first Strahler order; II: second Strahler order; III: third Strahler order); sampling depth: numbers indicates cm of depth beneath the streambed (10, 25 and 45); habitats type (A: riffle head; B: riffle tail; C: lateral side of pools; D1: bars: D2: curves). CHIR: Chiromidae; DIXI: Dixidae; oCERA: other Ceratopogonidae; CULI: Culicoides; LEPT: Leptoconops; MARU: Maruina; TIPU: Tipulidae; SIMU: Simulidae; PSYC: Psychodidae; dLARV: Elmidae Larva d; NEOE: Neoelmis; DYTI: Dytiscidae; PERL: Perlidae; niEPHE: non identified Ephemeroptera; BAET: Baetidae; LEPT: Leptophlebiidae; OECE: Oecetis; NECT: Nectopsiche; HELI: Helicopsiche; GRUM: Grumicha; MARI: Marlia; CYRN: Cyrnellus; HYDR: Hydroptilidae; COLL: Collembola; CYCL: Cyclopoida; PARA: Parastenocarididae; Ahar: Harpacticoida morphotype "a"; OSTR: Ostracoda; CHYD: Chidoridae; BATH: Bathynellacea; HYIA: Hydrachnidia; NEMA: Nematoda; ANN: Annelida. ID Site CHIR DIXI oCERA CULI LEPT MARU TIPU SIMU PSYC dLARV NEOE DYTI PERL niEPHE BAET LEPT OECE NECT HELI GRUM MARI CYRN HYDR COLL CYCL PARA Ahar OSTR CHYD BATH HYIA NEMA ANNE 26 I10A 5 0 0 5 0 0 3 0 0 0 2 0 0 0 0 0 0 0 0 0 0 2 0 0 1 0 4 1 0 0 4 0 4 27 I10B 12 0 0 17 1 1 0 0 1 0 0 0 0 2 0 0 1 0 0 0 0 0 0 1 1 0 14 1 0 0 14 0 1 28 I10C 20 0 0 3 0 0 1 0 0 0 0 0 0 0 2 0 0 0 0 2 0 0 0 0 0 0 9 4 1 0 5 2 8 29 I10D1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 1 2 1 30 I10D2 7 0 0 2 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 3 0 0 31 125IA 3 0 0 2 0 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 1 0 0 4 1 1 32 125B 3 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 2 3 5 33 I25C 4 0 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 10 1 4 0 1 0 4 1 3 34 125D1 7 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 1 0 0 0 1 0 0 2 11 35 I25D2 2 0 0 1 0 0 2 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 2 36 I45A 5 0 0 2 0 0 1 3 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 2 4 7 0 0 7 9 2 37 I45B 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 10 1 1 1 0 0 3 0 2 38 I45C 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 5 0 0 39 I45D1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 3 0 0 40 I45D2 1 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 3 0 0 0 0 1 1 1 II10A 6 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 1 0 2 0 0 9 4 2 2 II10B 15 0 0 14 0 0 3 0 0 0 0 0 1 2 0 0 0 0 0 0 0 0 0 0 6 9 9 12 14 0 7 17 61 3 II10C 21 0 0 0 0 0 1 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 25 7 5 3 13 0 9 4 4 4 II10D1 27 0 0 3 0 0 3 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 27 4 5 0 2 0 7 1 20 5 II10D2 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 6 II25A 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 1 1 7 II25B 42 0 6 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 2 7 7 1 0 3 0 6 6 0 8 II25C 30 0 2 0 0 0 0 0 0 0 1 0 0 2 0 0 0 0 0 0 1 0 0 0 1 29 1 0 3 0 13 1 0 9 II25D1 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 1 1 0 10 II25D2 3 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 1 0 11 II45A 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 14 2 1 3 12 II45B 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 1 0 13 II45C 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 6 0 8 3 5 1 1 3 5 14 II45D1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 9 0 1 0 0 1 2 0 1 15 II45D2 7 1 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 1 0 3 0 1 0 1 1 0 16 III10A 17 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 2 2 4 2 11 0 9 14 1 17 III10B 21 0 0 0 0 0 0 0 0 0 1 0 0 0 3 0 0 0 0 0 0 0 0 0 8 1 6 7 13 0 14 5 4 18 III10C 15 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 2 1 0 0 0 0 0 0 2 19 III10D1 24 0 0 3 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 1 0 1 1 0 0 7 2 1 20 III10D2 36 0 0 2 2 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 2 3 4 2 0 12 18 10 21 III25A 7 0 0 4 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 2 2 0 0 0 5 5 4 22 III25B 7 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 2 23 III25C 5 0 0 1 0 0 0 0 0 0 3 0 0 0 0 0 0 0 1 0 0 0 0 0 1 4 0 2 7 0 2 1 0 24 III25D1 4 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 1 0 0 0 6 0 0 25 III25D2 3 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 4 0 1 1 4 0 2 3 2 . A total of 31 taxa were identified belonging to Nematoda, Annelida, Crustacea, Hydrachnidia and Insecta. Insects were dominant with 23 taxa. A total of 1460 specimens were collected overall, of which 549 belonging to Insecta, 458 to Crustacea, and the remnants evenly distributed among Nematoda, Annelida and Hydrachnidia. The absolute abundances ranged from 4 to 170 individuals/site. Insects were not equally distributed among the various orders and families, being Chironomidae (Diptera) dominant with 369 individuals. The other 14 identified families of taxon Insecta accounted 180 individuals, overall. Copepods abundances accounted for 307 individuals; the rest of crustaceans, 151 individuals, were distributed in Cladocera, Ostracoda and Bathynellacea.

Both Shannon (H’) and Simpson (D) indices showed higher values at 45 cm in depth (H’ = 2.5; D = 0.9), while the lowest value was observed in the microhabitat represented by bars of sand accumulation (H’ = 2.1; D = 0.8). However, the ranges of the value of the indices were very narrow, indicating no marked differences in diversity indices among the orders of the reaches, depths and microhabitats, when considering all taxa. Conversely, the hyporheic assemblage showed clear spatial distribution in terms of abundances. Overall insect abundances significantly differed with depth (p<0.001), being higher at 10 cm than at the other two sampling depths (Figure 3). This pattern is mainly due to Diptera abundances (p<0.001), and above all to Chironomidae (p<0.001), whose abundances were significantly different at all depths, and to a lesser extent to Ephemeroptera that had higher abundances at 10 cm, being almost absent at the other depths. Insect abundances did not show a significant pattern considering stream orders and microhabitat typology according to the Kruskal_Wallis test. Water mite abundances were significantly higher at 10 cm (p-value<0.001), compared to the other two depths. The abundances of the taxon Crustacea showed a pattern influenced by microhabitat typology (p-value = 0.049), being higher in riffle tails and in lateral sides of pools. The remnant taxa abundances were not explained by the examined factors. Taxa richness, both total and measured for each higher taxa (Insecta, Crustacea, etc.), did not differ significantly either according to stream orders, or to habitats, or to depth. The first two axes of PCoA plot accounted for 46% of the total cumulative variation (30.3% axis 1 and 15.8% axis 2, respectively). The major part of taxa, with the predominance of Chironomidae and Hydracnidia, showed higher abundances along the negative axis 1 where most of the sites at the lowest depth (10 cm), were located (Figure 4).

Figure 3
Boxplot indicating differences in insect abundances at the three depths. Number of individuals on the Y axis.
Figure 4
Principal Coordinates Analysis on log-transformed species abundance data of the 40 sampling sites in the HZ of the Tijuca River. Left) Plot showing both the site locations of at different depth (black triangles: –10 cm; dark gray x: –25 cm; light gray quadrats: –45 cm) and species ordination overlain. Right) Plot showing the abundances of taxon Chironomidae at each sampling site. Diameter of circles are proportional to number of chironomids collected in each site.

5 Discussion

Studies on HZ in the Neotropical Region are virtually absent and the ecology of interstitial habitats along the rivers remains uninvestigated. The study of hyporheic assemblages is of particular interest due to the ability of hyporheic communities to provide signals of declining water quality (Hancock et al., 2005Hancock, P.J., Boulton, A.J. and Humphreys, W.F., 2005. Aquifers and hyporheic zones: towards an ecological understanding of groundwater. Hydrogeology Journal, vol. 13, no. 1, pp. 98-111. http://dx.doi.org/10.1007/s10040-004-0421-6.
http://dx.doi.org/10.1007/s10040-004-042...
; Di Marzio et al., 2009Di Marzio, W.D., Castaldo, D., Pantani, C., Di Cioccio, A., Di Lorenzo, T., Sáenz, M.E. and Galassi, D.M.P., 2009. Relative sensitivity of hyporheic copepods to chemicals. Bulletin of Environmental Contamination and Toxicology, vol. 82, no. 4, pp. 488-491. http://dx.doi.org/10.1007/s00128-008-9603-6. PMid:19005609.
http://dx.doi.org/10.1007/s00128-008-960...
; Iepure et al., 2013Iepure, S., Martinez-Hernandez, V., Herrera, S., Rasines-Ladero, R. and De Bustamante, I., 2013. Response of microcrustacean communities from the surface-groundwater interface to water contamination in urban river system of the Jarama basin (central Spain). Environmental Science and Pollution Research International, vol. 20, no. 8, pp. 5813-5826. http://dx.doi.org/10.1007/s11356-013-1529-9. PMid:23475443.
http://dx.doi.org/10.1007/s11356-013-152...
and references herein). In the Neotropical Region, the first study of interstitial fauna was accomplished by Fernández and Palacios (1989)Fernández, H.R. and Palacios, A.N., 1989. La fauna intersticial hiporreica dos rıos de montaña del noroeste de Argentina. Rivista di Idrobiologia, vol. 28, pp. 231-246. using the collecting method Chamaran-Chapuis (Chappuis, 1942Chappuis, P.A., 1942. Eine neue Methode zur Untersuchung der Grundwasser-Fauna. Acta Scientiarum Mathematicarum Naturalium (Unviersitatis Francisco-Josephina) Kolozsvar, vol. 6, pp. 1-7.). Fernández (1993Fernández, H.R., 1993. Acaros Intersticiales del Noroeste Argentino IV. Análisis filogenético y biogeográfico de Cook (Acari, Omartacaridae): una primera aproximación. OmartacarusRevista de la Sociedad Entomológica Argentina, vol. 52, pp. 107-117., 1994Fernández, H.R., 1994. Acaros Intersticiales del Noroeste Argentino III. Nuevos aportes morfológicos sobre especies hiporreicas del Lundblad y . ProtolimnesiaDiamphidaxona CookPhysis (Rio de Janeiro, Brazil), vol. 49, pp. 23-30., 2001Fernández, H.R., 2001. Acaros hiporreicos de Argentina: nuevos datos sobre Neomamersinae Lundblad (Limnesiidae). Physis (Rio de Janeiro, Brazil), vol. 58, pp. 21-28.) published a sequence of papers on interstitial water mites using the Bou-Rouch method (Bou, 1974Bou, C., 1974. Les methodes de récolte dans les eaux souterraines interstitielles. Annales de spéléologie, vol. 29, no. 4, pp. 611-619.). Both studies occurred in streams in Argentina. In other countries, studies mainly dealt with water chemistry and water flow exchanges in the HZ only (e.g. Chestnut and McDowell, 2000Chestnut, T.J. and McDowell, W.H., 2000. C and N dynamics in the riparian and hyporheic zones of a tropical stream, Luquillo Mountains, Puerto Rico. Journal of the North American Benthological Society, vol. 19, no. 2, pp. 199-214. http://dx.doi.org/10.2307/1468065.
http://dx.doi.org/10.2307/1468065...
; Romero-González et al., 2001Romero-González, M.E., Zambrano, E., Mesa, J. and Medina, H.L., 2001. Fractional phosphate composition in sediments from a tropical river (Catatumbo River, Venezuela). Hydrobiologia, vol. 450, no. 1-3, pp. 47-55. http://dx.doi.org/10.1023/A:1017535216608.
http://dx.doi.org/10.1023/A:101753521660...
; Medina et al., 2003Medina, H.L., De. Marín, J.C., Gutiérrez, E. and Morales, J., 2003. Nitrogen mobility at the sediment-water interface of Lake Maracaibo, Venezuela. Water, Air, and Soil Pollution, vol. 145, no. 1-4, pp. 341-357. http://dx.doi.org/10.1023/A:1023632702886.
http://dx.doi.org/10.1023/A:102363270288...
; De Smedt et al., 2006De Smedt, F., Brevis, W. and Debels, P., 2006. Analytical solution for solute transport resulting from instantaneous injection in streams with transient storage. Journal of Hydrology (Amsterdam), vol. 330, no. 3-4, pp. 759-760.; De Smedt, 2007De Smedt, F., 2007. Analytical solution and analysis of solute transport in rivers affected by diffusive transfer in the hyporheic zone. Journal of Hydrology (Amsterdam), vol. 339, no. 1-2, pp. 29-38. http://dx.doi.org/10.1016/j.jhydrol.2007.02.002.
http://dx.doi.org/10.1016/j.jhydrol.2007...
; Fabian et al., 2011Fabian, M.W., Endreny, T.A., Bottacin-Busolin, A. and Lautz, L.K., 2011. Seasonal variation in cascade-driven hyporheic exchange, northern Honduras. Hydrological Processes, vol. 25, no. 10, pp. 1630-1646. http://dx.doi.org/10.1002/hyp.7924.
http://dx.doi.org/10.1002/hyp.7924...
; Cuajinicuilapa et al., 2012Cuajinicuilapa, D., Sandoval, C. and Cuajinicuilapa, D., 2012. Evidencias de interacción entre aguas superficiales y subterráneas. Revista Internacional de Estadistica y Geografia., vol. 3, no. 2, pp. 116-129.; Marchetti and Carrillo-Rivera, 2013Marchetti, Z.Y. and Carrillo-Rivera, J.J., 2013. Tracing groundwater discharge in the floodplain of the parana river, argentina: implications for its biological communities. River Research and Applications, http://dx.doi.org/10.1002/rra.2629.
http://dx.doi.org/10.1002/rra.2629...
).

In our survey, the sampling sites located in the reach PIII at the depth of 45 cm were unsaturated. This fact may be due to the presence of an upstream cascade followed by a small dam of 1.5 m in height. Dams along small-order streams are known to alter the linkage between headwater and downstream reaches, potentially increasing at short distance hyporheic connectivity in the riparian zone (Duke et al., 2007Duke, J.R., White, J.D., Allen, P.M. and Muttiah, R.S., 2007. Riparian influence on hyporheic-zone formation downstream of a small dam in the Blackland Prairie region of Texas. Hydrological Processes, vol. 21, no. 2, pp. 141-150. http://dx.doi.org/10.1002/hyp.6228.
http://dx.doi.org/10.1002/hyp.6228...
). In particular, dams simplify alluvial system structure, reducing surface water peak flows and hyporheic flow and thus preventing refilling of alluvial aquifers (Berman and Pole, 2000Berman, G.C. and Pole, C.H., 2000. Pathways of human influence on water temperature dynamics in stream channels. Environmental Management, vol. 1, pp. 1-20.).

The upper layers of HZ of Tijuca River were dominated by insects, particularly Chironomidae. This pattern copes with data from other studies, since insects are known to use HZ to seek for refuge during periods of disturbance (Sedell et al., 1990Sedell, J.R., Reeves, G.H., Hauer, F.R., Stanford, J.A. and Hawkins, C.P., 1990. Role of refugia in recovery from disturbances: modern fragmented and disconnected river systems. Environmental Management, vol. 14, no. 5, pp. 711-724. http://dx.doi.org/10.1007/BF02394720.
http://dx.doi.org/10.1007/BF02394720...
; Robertson et al., 1995Robertson, A.L., Lancaster, J. and Hildrew, A.G., 1995. Stream hydraulics and the distribution of microcrustacea: A role for refugia? Freshwater Biology, vol. 33, no. 3, pp. 469-484. http://dx.doi.org/10.1111/j.1365-2427.1995.tb00407.x.
http://dx.doi.org/10.1111/j.1365-2427.19...
; Dole-Olivier et al., 1997Dole-OlivIer, M.J., Marmonier, P. and Beffy, J.L., 1997. Response of invertebrate to lotic disturbance: is the hyporheic zone a patchy refugium? Freshwater Biology, vol. 37, no. 2, pp. 257-276. http://dx.doi.org/10.1046/j.1365-2427.1997.00140.x.
http://dx.doi.org/10.1046/j.1365-2427.19...
) or to find more stable habitats (Matthaei et al., 2000Matthaei, C.D., Arbuckle, C.J. and Townsend, C.R., 2000. Stable surface stones as refugia for invertebrates during disturbance in a New Zealand stream. Journal of the North American Benthological Society, vol. 19, no. 1, pp. 82-93. http://dx.doi.org/10.2307/1468283.
http://dx.doi.org/10.2307/1468283...
; Fowler and Death, 2001Fowler, R.T. and Death, R.G., 2001. The effect of environmental stability on hyporheic community structure. Hydrobiologia, vol. 445, no. 1/3, pp. 85-95. http://dx.doi.org/10.1023/A:1017507404733.
http://dx.doi.org/10.1023/A:101750740473...
). Dole-Olivier (2011)Dole-Olivier, M.J., 2011. The hyporheic refuge hypothesis reconsidered: a review of hydrological aspects. Marine & Freshwater Research, vol. 62, no. 11, pp. 1281-1302. http://dx.doi.org/10.1071/MF11084.
http://dx.doi.org/10.1071/MF11084...
reviewed the importance of the HZ as a protected "nursery" for eggs, early instar larvae, and quiescent stages of benthic invertebrates as Plecoptera, Ephemeroptera and Chironomidae. The Chironomidae were observed to be the most common insect in interstitial zone (Resh and Rosenberg, 1984Resh, H.R. and Rosenberg, D.M., 1984. The ecology of aquatic insects. New York: Praeger Publishers. 625 p.; Ferrington Junior, 2008Ferrington Junior, L.C., 2008. Global diversity of non-biting midges (Chironomidae; Insecta-Diptera) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 447-455. http://dx.doi.org/10.1007/s10750-007-9130-1.
http://dx.doi.org/10.1007/s10750-007-913...
). They play a particularly important role in stream dynamics (Coffman and Ferrington Junior, 1996Coffman, W.P. and Ferrington Junior, L.C., 1996. Chironomidae. In: R.W. MERRITT and K.W. CUMMINS eds. An introduction to the aquatic insects of North America. 3rd ed. Dubuque: Kendall/Hunt, pp. 635-754.) and may be an important component of hyporheos (Lencioni et al., 2008Lencioni, V., Marziali, L. and Rossaro, B., 2008. Hyporheic chironomids in alpine streams. Boletim do Museu Municipal do Funchal, vol. 13, pp. 127-132.). They typically are confined to surface sediment, but some species can penetrate deeper (Pinder, 1986Pinder, L.C.V., 1986. Biology of freshwater chironomidae. Annual Review of Entomology, vol. 31, no. 1, pp. 1-23. http://dx.doi.org/10.1146/annurev.en.31.010186.000245.
http://dx.doi.org/10.1146/annurev.en.31....
) and larvae have been found invading the HZ at depths of up to 2 m, following high discharge events (Dole-Olivier et al., 1997Dole-OlivIer, M.J., Marmonier, P. and Beffy, J.L., 1997. Response of invertebrate to lotic disturbance: is the hyporheic zone a patchy refugium? Freshwater Biology, vol. 37, no. 2, pp. 257-276. http://dx.doi.org/10.1046/j.1365-2427.1997.00140.x.
http://dx.doi.org/10.1046/j.1365-2427.19...
). This strategy may in part account for the high resistance of these taxa to flood event (Anderson and Ferrington, 2012Anderson, A.M. and Ferrington, L.C., 2012. Resistance and resilience of winter-emerging Chironomidae (Diptera) to a flood event: implications for Minnesota trout streams. Hydrobiologia, vol. 707, no. 1, pp. 59-71. http://dx.doi.org/10.1007/s10750-012-1406-4.
http://dx.doi.org/10.1007/s10750-012-140...
).

In our study, water mites were found with the highest abundances in the upper layers of the HZ of the Tijuca River. In surface water habitats, Hydrachnidia can be very abundant and diverse (Smith and Cook, 1991Smith, I.M. and COOK, D.R. 1991. Water mites. In: J.H. THORP and A.P. COVICH, eds. Ecology and classification of North American freshwater invertebrates. San Diego: Academic Press, pp. 523-592.; Di Sabatino et al., 2000Di Sabatino, A., Gerecke, R. and Martin, P., 2000. The Biology and Ecology of lotic water mites (Hydrachnidia). Freshwater Biology, vol. 44, no. 1, pp. 47-62. http://dx.doi.org/10.1046/j.1365-2427.2000.00591.x.
http://dx.doi.org/10.1046/j.1365-2427.20...
). In general, in the HZ they are less abundant, although in some case they can show a diversity compared with other meiofaunal groups (Di Sabatino et al., 2000Di Sabatino, A., Gerecke, R. and Martin, P., 2000. The Biology and Ecology of lotic water mites (Hydrachnidia). Freshwater Biology, vol. 44, no. 1, pp. 47-62. http://dx.doi.org/10.1046/j.1365-2427.2000.00591.x.
http://dx.doi.org/10.1046/j.1365-2427.20...
). In the Neotropical Region many species are able to exploit both benthic layers and the HZ of lotic systems with frequent vertical migrations (Fernández and Fossati-Gaschignard, 2011Fernández, H.R. and Fossati-Gaschignard, O., 2011. An initial classification of Neotropical water mites (Acari: Hydrachnidia) based on habitat preferences. International Journal of Ecology, vol. 2011, pp. 1-11. http://dx.doi.org/10.1155/2011/910540.
http://dx.doi.org/10.1155/2011/910540...
). Identification to species level and further investigations are required in order to better explain the pattern highlighted in this study. Oligochaetes and nematods were fairly represented in the HZ of the Tijuca River, although they were not dominant as previously observed in other studies (Mary and Marmonier, 2000Mary, N. and Marmonier, P., 2000. First survey of interstitial fauna in New Caledonian rivers: influence of geological and geomorphological characteristics. Hydrobiologia, vol. 418, no. 1, pp. 199-208. http://dx.doi.org/10.1023/A:1003938629671.
http://dx.doi.org/10.1023/A:100393862967...
; Lafont and Vivier, 2006Lafont, M. and Vivier, A., 2006. Oligochaete assemblages in the hyporheic zone and coarse surface sediments: their importance for understanding of ecological functioning of watercourses. Hydrobiologia, vol. 564, no. 1, pp. 171-181. http://dx.doi.org/10.1007/s10750-005-1717-9.
http://dx.doi.org/10.1007/s10750-005-171...
). The high abundances in the HZ may be favoured by the worm-shaped body, that facilitates the movement in the interstices of HZ sediments (Omesová and Helešic, 2007Omesová, M. and Helešic, J., 2007. Vertical Distribution of Invertebrates in Bed Sediments of a Gravel Stream in the Czech Republic. International Review of Hydrobiology, vol. 92, no. 4-5, pp. 480-490. http://dx.doi.org/10.1002/iroh.200610990.
http://dx.doi.org/10.1002/iroh.200610990...
; Omesová et al., 2008Omesová, M., Horsák, M. and Helešic, J., 2008. Nested patterns in hyporheic meta-communities : the role of body morphology and penetrability of sediment. Naturwissenschaften, vol. 95, no. 10, pp. 917-926. http://dx.doi.org/10.1007/s00114-008-0399-3. PMid:18542903.
http://dx.doi.org/10.1007/s00114-008-039...
). Crustaceans, in particular copepods, ostracods and cladocerans, can be both abundant and species-rich in running waters and HZ (Dole-Olivier et al., 2000Dole-Olivier, M.-J., Galassi, D.M.P., Marmonier, P. and Creuzé des Châtelliers, M., 2000. The biology and ecology of lotic microcrustaceans. Freshwater Biology, vol. 44, no. 1, pp. 63-91. http://dx.doi.org/10.1046/j.1365-2427.2000.00590.x.
http://dx.doi.org/10.1046/j.1365-2427.20...
; Galassi, 2001Galassi, D.M.P., 2001. Groundwater copepods (Crustacea: Copepoda): diversity patterns over ecological and evolutionary scales. Hydrobiologia, vol. 453/454, pp. 227-253. http://dx.doi.org/10.1023/A:1013100924948.
http://dx.doi.org/10.1023/A:101310092494...
). Only seven known species of cladocerans may be regarded as true inhabitants of subterranean environments, although they actively colonize ecotonal habitats (Forró et al., 2008Forró, L., Korovchinsky, N.M., Kotov, A.A. and Petrusek, A., 2008. Global diversity of cladocerans (Cladocera; Crustacea) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 177-184. http://dx.doi.org/10.1007/s10750-007-9013-5.
http://dx.doi.org/10.1007/s10750-007-901...
). Van Damme et al. (2009)Van Damme, K., Brancelj, A. and Dumont, H.J., 2009. Adaptations to the hyporheic in Aloninae (Crustacea: Cladocera): allocation of Alona protzi Hartwig, 1900 and related species to Phreatalona gen. nov. Hydrobiologia, vol. 618, no. 1, pp. 1-34. http://dx.doi.org/10.1007/s10750-008-9607-6.
http://dx.doi.org/10.1007/s10750-008-960...
found specimens of Chidoridae up to a depth of 60 cm beneath the riverbed. In our samples, cladocerans were distributed at all depths, although they were mainly found in the upper layers (68% at 10 cm). In our study, copepods were the most abundant crustaceans. A similar condition was observed by other authors (Boulton et al., 1992Boulton, A.J., Valett, H.M. and Fisher, S.G., 1992. Spatial distribution and taxonomic composition of the hyporheos of several Sonoran Desert streams. Archiv für Hydrobiologie, vol. 125, pp. 37-61.; Hunt and Stanley, 2003Hunt, G.W. and Stanley, E.H., 2003. Environmental factors influencing the composition and distribution of the hyporheic in Oklahoma streams: variation across ecoregions. Archiv für Hydrobiologie, vol. 158, no. 1, pp. 1-24. http://dx.doi.org/10.1127/0003-9136/2003/0158-0001.
http://dx.doi.org/10.1127/0003-9136/2003...
; Di Lorenzo et al., 2013Di Lorenzo, T., Stoch, F. and Galassi, D.M.P., 2013. Incorporating the hyporheic zone within the river discontinuum: longitudinal patterns of subsurface copepod assemblages in an Alpine stream. Limnologica, vol. 43, no. 4, pp. 288-296. http://dx.doi.org/10.1016/j.limno.2012.12.003.
http://dx.doi.org/10.1016/j.limno.2012.1...
and references herein). Harpacticoids are mainly burrowers and often dominant in HZ due to their holobenthonic lifecycle (Dole-Olivier et al., 2000Dole-Olivier, M.-J., Galassi, D.M.P., Marmonier, P. and Creuzé des Châtelliers, M., 2000. The biology and ecology of lotic microcrustaceans. Freshwater Biology, vol. 44, no. 1, pp. 63-91. http://dx.doi.org/10.1046/j.1365-2427.2000.00590.x.
http://dx.doi.org/10.1046/j.1365-2427.20...
; Galassi, 2001Galassi, D.M.P., 2001. Groundwater copepods (Crustacea: Copepoda): diversity patterns over ecological and evolutionary scales. Hydrobiologia, vol. 453/454, pp. 227-253. http://dx.doi.org/10.1023/A:1013100924948.
http://dx.doi.org/10.1023/A:101310092494...
). Cyclopods are also common in benthic and HZ habitats (Dole-Olivier et al., 2000Dole-Olivier, M.-J., Galassi, D.M.P., Marmonier, P. and Creuzé des Châtelliers, M., 2000. The biology and ecology of lotic microcrustaceans. Freshwater Biology, vol. 44, no. 1, pp. 63-91. http://dx.doi.org/10.1046/j.1365-2427.2000.00590.x.
http://dx.doi.org/10.1046/j.1365-2427.20...
; Galassi, 2001Galassi, D.M.P., 2001. Groundwater copepods (Crustacea: Copepoda): diversity patterns over ecological and evolutionary scales. Hydrobiologia, vol. 453/454, pp. 227-253. http://dx.doi.org/10.1023/A:1013100924948.
http://dx.doi.org/10.1023/A:101310092494...
; Brancelj and Dumont, 2007Brancelj, A. and Dumont, H.J., 2007. A review of the diversity, adaptations and groundwater colonization pathways in Cladocera and Calanoida (Crustacea), two rare and contrasting groups of stygobionts. Fundamental of Applied Limnology., vol. 168, no. 1, pp. 3-17. http://dx.doi.org/10.1127/1863-9135/2007/0168-0003.
http://dx.doi.org/10.1127/1863-9135/2007...
; Galassi et al., 2009Galassi, D.M.P., Huys, R. and Reid, J.W., 2009. Diversity, ecology and evolution of groundwater copepods. Freshwater Biology, vol. 54, no. 4, pp. 691-708. http://dx.doi.org/10.1111/j.1365-2427.2009.02185.x.
http://dx.doi.org/10.1111/j.1365-2427.20...
), although they prefer coarse sediments. Copepod abundances, mainly related to cyclopoids, were higher in the riffle-tail and pool habitats of the HZ of the Tijuca River, where upwelling of ground water was supposed to be consistent (Dole-Olivier, 1998Dole-Olivier, M.J., 1998. Surface water/groundwater exchanges in three dimensions on a backwater of the Rhône river. Freshwater Biology, vol. 40, no. 1, pp. 93-109. http://dx.doi.org/10.1046/j.1365-2427.1998.00335.x.
http://dx.doi.org/10.1046/j.1365-2427.19...
). A similar result was found by Mori and Brancelj (2011)Mori, N. and Brancelj, A., 2011. Spatial and temporal variability of hyporheic invertebrate community within a stream reach of the River Bača (W Slovenia). Natura Sloveniae, vol. 13, no. 1, pp. 25-38.. According to this, the high abundances observed in this survey might be due to the massive presence of stygobiotic species. However, identifications to species level are required in order to shed light on this hypothesis. The occurrence of specimens from Parastenocarididae (Copepoda, Harpacticoida) in the HZ of the Tijuca River requires special mention. At present, the family includes five genera, four of which are exclusively found in the Neotropical Region (Galassi, 2001Galassi, D.M.P., 2001. Groundwater copepods (Crustacea: Copepoda): diversity patterns over ecological and evolutionary scales. Hydrobiologia, vol. 453/454, pp. 227-253. http://dx.doi.org/10.1023/A:1013100924948.
http://dx.doi.org/10.1023/A:101310092494...
). In the HZ of the Tijuca River, specimens of Parastenocarididae were mainly collected in the sandier reach PII (60% of sand in the streambed). Bathynellacea (Syncarida) are stygobionts (Camacho and Valdecasas, 2008Camacho, A.I. and Valdecasas, A.G., 2008. Global diversity of syncarids (Syncarida; Crustacea) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 257-266. http://dx.doi.org/10.1007/s10750-007-9021-5.
http://dx.doi.org/10.1007/s10750-007-902...
). They were only found in the deeper layers of the HZ in our survey. Remarkably, Amphipoda and Isopoda were not found in this first investigation. However, their presence cannot be excluded and further surveys are necessary.

6 Conclusions

The research in the HZ in Neotropical Region is still a challenge due to the paucity of basic information. The ecology of many invertebrate taxa found in the HZ of neotropical streams is almost unknown, especially for amphibite species. Only a few stygobiont species were described up to now. The results of this study represent new data about hyporheic invertebrate assemblages in this region. Seasonal surveys in the HZ of the Tijuca River are required in order to confirm the distribution patterns highlighted in this study. The analysis of other abiotic variables, such as granulometry, organic matter content and chemical-physical conditions, might highlight new patterns and better explain those analyzed in this first survey. Identification at species level is required for hyporheic specimens, in order to allow the attribution of the species either to the stygobiotic or non-stygobiotic categories, in this way obtaining a better assessment and understanding of the HZ biodiversity.

Appendix 1 Sampling sites and taxa abundances (number of individuals). Site codes include information about: Strahler order (I: first Strahler order; II: second Strahler order; III: third Strahler order); sampling depth: numbers indicates cm of depth beneath the streambed (10, 25 and 45); habitats type (A: riffle head; B: riffle tail; C: lateral side of pools; D1: bars: D2: curves). CHIR: Chiromidae; DIXI: Dixidae; oCERA: other Ceratopogonidae; CULI: Culicoides; LEPT: Leptoconops; MARU: Maruina; TIPU: Tipulidae; SIMU: Simulidae; PSYC: Psychodidae; dLARV: Elmidae Larva d; NEOE: Neoelmis; DYTI: Dytiscidae; PERL: Perlidae; niEPHE: non identified Ephemeroptera; BAET: Baetidae; LEPT: Leptophlebiidae; OECE: Oecetis; NECT: Nectopsiche; HELI: Helicopsiche; GRUM: Grumicha; MARI: Marlia; CYRN: Cyrnellus; HYDR: Hydroptilidae; COLL: Collembola; CYCL: Cyclopoida; PARA: Parastenocarididae; Ahar: Harpacticoida morphotype "a"; OSTR: Ostracoda; CHYD: Chidoridae; BATH: Bathynellacea; HYIA: Hydrachnidia; NEMA: Nematoda; ANN: Annelida.

ID Site CHIR DIXI oCERA CULI LEPT MARU TIPU SIMU PSYC dLARV NEOE DYTI PERL niEPHE BAET LEPT OECE NECT HELI GRUM MARI CYRN HYDR COLL CYCL PARA Ahar OSTR CHYD BATH HYIA NEMA ANNE
26 I10A 5 0 0 5 0 0 3 0 0 0 2 0 0 0 0 0 0 0 0 0 0 2 0 0 1 0 4 1 0 0 4 0 4
27 I10B 12 0 0 17 1 1 0 0 1 0 0 0 0 2 0 0 1 0 0 0 0 0 0 1 1 0 14 1 0 0 14 0 1
28 I10C 20 0 0 3 0 0 1 0 0 0 0 0 0 0 2 0 0 0 0 2 0 0 0 0 0 0 9 4 1 0 5 2 8
29 I10D1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 1 2 1
30 I10D2 7 0 0 2 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 3 0 0
31 125IA 3 0 0 2 0 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 4 1 0 0 4 1 1
32 125B 3 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 2 3 5
33 I25C 4 0 1 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 10 1 4 0 1 0 4 1 3
34 125D1 7 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 1 0 0 0 1 0 0 2 11
35 I25D2 2 0 0 1 0 0 2 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 2
36 I45A 5 0 0 2 0 0 1 3 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 1 2 4 7 0 0 7 9 2
37 I45B 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 10 1 1 1 0 0 3 0 2
38 I45C 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0 0 5 0 0
39 I45D1 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 3 0 0
40 I45D2 1 0 0 1 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 3 0 0 0 0 1 1
1 II10A 6 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 1 0 2 0 0 9 4 2
2 II10B 15 0 0 14 0 0 3 0 0 0 0 0 1 2 0 0 0 0 0 0 0 0 0 0 6 9 9 12 14 0 7 17 61
3 II10C 21 0 0 0 0 0 1 0 0 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 25 7 5 3 13 0 9 4 4
4 II10D1 27 0 0 3 0 0 3 0 0 0 0 0 0 0 0 3 0 0 0 0 0 0 0 0 27 4 5 0 2 0 7 1 20
5 II10D2 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 0 0
6 II25A 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 0 0 1 1
7 II25B 42 0 6 0 0 0 1 0 0 0 0 0 0 0 0 1 0 0 0 0 1 0 0 2 7 7 1 0 3 0 6 6 0
8 II25C 30 0 2 0 0 0 0 0 0 0 1 0 0 2 0 0 0 0 0 0 1 0 0 0 1 29 1 0 3 0 13 1 0
9 II25D1 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 0 1 1 0
10 II25D2 3 0 0 1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 3 1 0
11 II45A 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 1 0 0 14 2 1 3
12 II45B 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 1 0 0 1 0
13 II45C 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 6 0 8 3 5 1 1 3 5
14 II45D1 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 1 9 0 1 0 0 1 2 0 1
15 II45D2 7 1 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 1 0 3 0 1 0 1 1 0
16 III10A 17 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 0 0 2 2 4 2 11 0 9 14 1
17 III10B 21 0 0 0 0 0 0 0 0 0 1 0 0 0 3 0 0 0 0 0 0 0 0 0 8 1 6 7 13 0 14 5 4
18 III10C 15 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 0 0 0 0 2 1 0 0 0 0 0 0 2
19 III10D1 24 0 0 3 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 1 1 0 1 1 0 0 7 2 1
20 III10D2 36 0 0 2 2 0 1 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 1 0 0 2 3 4 2 0 12 18 10
21 III25A 7 0 0 4 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 1 2 2 0 0 0 5 5 4
22 III25B 7 0 0 1 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 2
23 III25C 5 0 0 1 0 0 0 0 0 0 3 0 0 0 0 0 0 0 1 0 0 0 0 0 1 4 0 2 7 0 2 1 0
24 III25D1 4 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1 1 0 1 0 0 0 6 0 0
25 III25D2 3 0 0 0 0 0 0 0 0 0 0 0 0 0 1 0 0 0 0 0 0 0 0 0 4 0 1 1 4 0 2 3 2

Acknowledgements

We are indebted to CAPES and FAPERJ for the financial support. Many thanks to Dr. Kury Adriano Museu Nacional/UFRJ for allowing the research activities in the Aracnolory Laboratory and Gatti Mario Curator of Coleção Micológica de Trichocomaceae IOC/FIOCRUZ for the technical support.

  • (With 4 figures)

References

  • Anderson, A.M. and Ferrington, L.C., 2012. Resistance and resilience of winter-emerging Chironomidae (Diptera) to a flood event: implications for Minnesota trout streams. Hydrobiologia, vol. 707, no. 1, pp. 59-71. http://dx.doi.org/10.1007/s10750-012-1406-4.
    » http://dx.doi.org/10.1007/s10750-012-1406-4
  • Barbour, M.T., Gerritsen, J., Snyder, B.D. and Stribling, J.B., 1999. Rapid bioassessment protocols for use in streams and Wadeable Rivers: periphyton, benthic macroinvertebrates and fish. 2nd ed. Washington, D.C.: EPA. 197 p.
  • Bencala, K.E., 2000. Hyporheic zone hydrological processes. Hydrological Processes, vol. 14, no. 15, pp. 2797-2798. http://dx.doi.org/10.1002/1099-1085(20001030)14:15<2797::AID-HYP402>3.0.CO;2-6.
    » http://dx.doi.org/10.1002/1099-1085(20001030)14:15<2797::AID-HYP402>3.0.CO;2-6
  • Bencala, K.E., 2005. Hyporheic exchange flows. In: M.G. ANDERSON and J.J. MCDONNELL, eds. Encyclopedia of hydrological sciences. New Jersey: John Wiley and Sons, vol. 3, chap. 113, pp. 1733-1740.
  • Berman, G.C. and Pole, C.H., 2000. Pathways of human influence on water temperature dynamics in stream channels. Environmental Management, vol. 1, pp. 1-20.
  • Bou, C., 1974. Les methodes de récolte dans les eaux souterraines interstitielles. Annales de spéléologie, vol. 29, no. 4, pp. 611-619.
  • Boulton, A.J., Dole-Olivier, M.-J. and Marmonier, P., 2004. Effects of sample volume and taxonomic resolution on assessment of hyporheic assemblage composition sampled using a Bou-Rouch pump. Archiv für Hydrobiologie, vol. 159, no. 3, pp. 327-355. http://dx.doi.org/10.1127/0003-9136/2004/0159-0327.
    » http://dx.doi.org/10.1127/0003-9136/2004/0159-0327
  • Boulton, A.J., Findlay, S., Marmonier, P., Stanley, E.H. and Valett, M., 1998. The functional significance of the hyporheic zone in streams and rivers. Annual Review of Ecology and Systematics, vol. 29, no. 1, pp. 59-81. http://dx.doi.org/10.1146/annurev.ecolsys.29.1.59.
    » http://dx.doi.org/10.1146/annurev.ecolsys.29.1.59
  • Boulton, A.J., Marmonier, P. and Sarriquet, P.-E.X., 2007. Hyporheic invertebrate community composition in streams of varying salinity in south-western Australia: diversity peaks at intermediate thresholds. River Research and Applications, vol. 23, no. 6, pp. 579-594. http://dx.doi.org/10.1002/rra.989.
    » http://dx.doi.org/10.1002/rra.989
  • Boulton, A.J., Valett, H.M. and Fisher, S.G., 1992. Spatial distribution and taxonomic composition of the hyporheos of several Sonoran Desert streams. Archiv für Hydrobiologie, vol. 125, pp. 37-61.
  • Brancelj, A. and Dumont, H.J., 2007. A review of the diversity, adaptations and groundwater colonization pathways in Cladocera and Calanoida (Crustacea), two rare and contrasting groups of stygobionts. Fundamental of Applied Limnology., vol. 168, no. 1, pp. 3-17. http://dx.doi.org/10.1127/1863-9135/2007/0168-0003.
    » http://dx.doi.org/10.1127/1863-9135/2007/0168-0003
  • BRASIL. Ministério das Minas e Energia, 1987. Projeto Radambrasil: levantamento de recursos naturais. Rio de Janeiro: Ministério das Minas e Energia. vol. 32, 780 p.
  • Brooks, S.S. and Boulton, A.J., 1991. Recolonization dynamics of benthic macroinvertebrates after artificial and natural disturbances in an Australian temporary stream. Australian Journal of Marine and Freshwater Research, vol. 42, no. 3, pp. 295-308. http://dx.doi.org/10.1071/MF9910295.
    » http://dx.doi.org/10.1071/MF9910295
  • Brown, H.D., 1975. A counterstaining technique for use in sorting benthic sample? Limnology and Oceanography, vol. 19, pp. 152-154.
  • Brunke, M. and Gonser, T., 1997. The ecological significance of exchange processes between rivers and groundwater. Freshwater Biology, vol. 37, no. 1, pp. 1-33. http://dx.doi.org/10.1046/j.1365-2427.1997.00143.x.
    » http://dx.doi.org/10.1046/j.1365-2427.1997.00143.x
  • Camacho, A.I. and Valdecasas, A.G., 2008. Global diversity of syncarids (Syncarida; Crustacea) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 257-266. http://dx.doi.org/10.1007/s10750-007-9021-5.
    » http://dx.doi.org/10.1007/s10750-007-9021-5
  • Chappuis, P.A., 1942. Eine neue Methode zur Untersuchung der Grundwasser-Fauna. Acta Scientiarum Mathematicarum Naturalium (Unviersitatis Francisco-Josephina) Kolozsvar, vol. 6, pp. 1-7.
  • Chestnut, T.J. and McDowell, W.H., 2000. C and N dynamics in the riparian and hyporheic zones of a tropical stream, Luquillo Mountains, Puerto Rico. Journal of the North American Benthological Society, vol. 19, no. 2, pp. 199-214. http://dx.doi.org/10.2307/1468065.
    » http://dx.doi.org/10.2307/1468065
  • Coffman, W.P. and Ferrington Junior, L.C., 1996. Chironomidae. In: R.W. MERRITT and K.W. CUMMINS eds. An introduction to the aquatic insects of North America. 3rd ed. Dubuque: Kendall/Hunt, pp. 635-754.
  • Cuajinicuilapa, D., Sandoval, C. and Cuajinicuilapa, D., 2012. Evidencias de interacción entre aguas superficiales y subterráneas. Revista Internacional de Estadistica y Geografia., vol. 3, no. 2, pp. 116-129.
  • De Smedt, F., 2007. Analytical solution and analysis of solute transport in rivers affected by diffusive transfer in the hyporheic zone. Journal of Hydrology (Amsterdam), vol. 339, no. 1-2, pp. 29-38. http://dx.doi.org/10.1016/j.jhydrol.2007.02.002.
    » http://dx.doi.org/10.1016/j.jhydrol.2007.02.002
  • De Smedt, F., Brevis, W. and Debels, P., 2006. Analytical solution for solute transport resulting from instantaneous injection in streams with transient storage. Journal of Hydrology (Amsterdam), vol. 330, no. 3-4, pp. 759-760.
  • Di Lorenzo, T., Stoch, F. and Galassi, D.M.P., 2013. Incorporating the hyporheic zone within the river discontinuum: longitudinal patterns of subsurface copepod assemblages in an Alpine stream. Limnologica, vol. 43, no. 4, pp. 288-296. http://dx.doi.org/10.1016/j.limno.2012.12.003.
    » http://dx.doi.org/10.1016/j.limno.2012.12.003
  • Di Marzio, W.D., Castaldo, D., Pantani, C., Di Cioccio, A., Di Lorenzo, T., Sáenz, M.E. and Galassi, D.M.P., 2009. Relative sensitivity of hyporheic copepods to chemicals. Bulletin of Environmental Contamination and Toxicology, vol. 82, no. 4, pp. 488-491. http://dx.doi.org/10.1007/s00128-008-9603-6. PMid:19005609.
    » http://dx.doi.org/10.1007/s00128-008-9603-6
  • Di Sabatino, A., Gerecke, R. and Martin, P., 2000. The Biology and Ecology of lotic water mites (Hydrachnidia). Freshwater Biology, vol. 44, no. 1, pp. 47-62. http://dx.doi.org/10.1046/j.1365-2427.2000.00591.x.
    » http://dx.doi.org/10.1046/j.1365-2427.2000.00591.x
  • Dole-Olivier, M.J., 1998. Surface water/groundwater exchanges in three dimensions on a backwater of the Rhône river. Freshwater Biology, vol. 40, no. 1, pp. 93-109. http://dx.doi.org/10.1046/j.1365-2427.1998.00335.x.
    » http://dx.doi.org/10.1046/j.1365-2427.1998.00335.x
  • Dole-Olivier, M.J., 2011. The hyporheic refuge hypothesis reconsidered: a review of hydrological aspects. Marine & Freshwater Research, vol. 62, no. 11, pp. 1281-1302. http://dx.doi.org/10.1071/MF11084.
    » http://dx.doi.org/10.1071/MF11084
  • Dole-Olivier, M.-J., Galassi, D.M.P., Marmonier, P. and Creuzé des Châtelliers, M., 2000. The biology and ecology of lotic microcrustaceans. Freshwater Biology, vol. 44, no. 1, pp. 63-91. http://dx.doi.org/10.1046/j.1365-2427.2000.00590.x.
    » http://dx.doi.org/10.1046/j.1365-2427.2000.00590.x
  • Dole-OlivIer, M.J., Marmonier, P. and Beffy, J.L., 1997. Response of invertebrate to lotic disturbance: is the hyporheic zone a patchy refugium? Freshwater Biology, vol. 37, no. 2, pp. 257-276. http://dx.doi.org/10.1046/j.1365-2427.1997.00140.x.
    » http://dx.doi.org/10.1046/j.1365-2427.1997.00140.x
  • Duke, J.R., White, J.D., Allen, P.M. and Muttiah, R.S., 2007. Riparian influence on hyporheic-zone formation downstream of a small dam in the Blackland Prairie region of Texas. Hydrological Processes, vol. 21, no. 2, pp. 141-150. http://dx.doi.org/10.1002/hyp.6228.
    » http://dx.doi.org/10.1002/hyp.6228
  • ENVIRONMENT AGENCY – EA, 2009. The hyporheic handbook: a handbook on the groundwater-surface water interface and hyporheic zone for environment managers. Bristol: Environment Agency. Science Report, SC050070.
  • Fabian, M.W., Endreny, T.A., Bottacin-Busolin, A. and Lautz, L.K., 2011. Seasonal variation in cascade-driven hyporheic exchange, northern Honduras. Hydrological Processes, vol. 25, no. 10, pp. 1630-1646. http://dx.doi.org/10.1002/hyp.7924.
    » http://dx.doi.org/10.1002/hyp.7924
  • Fenoglio, S., Bo, T. and Bosi, G., 2006. Deep interstitial habitat as a refuge for Agabus paludosus (fabricius) (Coleoptera: Dytiscidae) during summer droughts. Coleopterists Bulletin, vol. 60, no. 1, pp. 37-41. http://dx.doi.org/10.1649/842.1.
    » http://dx.doi.org/10.1649/842.1
  • Fernández, H.R. and Fossati-Gaschignard, O., 2011. An initial classification of Neotropical water mites (Acari: Hydrachnidia) based on habitat preferences. International Journal of Ecology, vol. 2011, pp. 1-11. http://dx.doi.org/10.1155/2011/910540.
    » http://dx.doi.org/10.1155/2011/910540
  • Fernández, H.R. and Palacios, A.N., 1989. La fauna intersticial hiporreica dos rıos de montaña del noroeste de Argentina. Rivista di Idrobiologia, vol. 28, pp. 231-246.
  • Fernández, H.R., 1993. Acaros Intersticiales del Noroeste Argentino IV. Análisis filogenético y biogeográfico de Cook (Acari, Omartacaridae): una primera aproximación. OmartacarusRevista de la Sociedad Entomológica Argentina, vol. 52, pp. 107-117.
  • Fernández, H.R., 1994. Acaros Intersticiales del Noroeste Argentino III. Nuevos aportes morfológicos sobre especies hiporreicas del Lundblad y . ProtolimnesiaDiamphidaxona CookPhysis (Rio de Janeiro, Brazil), vol. 49, pp. 23-30.
  • Fernández, H.R., 2001. Acaros hiporreicos de Argentina: nuevos datos sobre Neomamersinae Lundblad (Limnesiidae). Physis (Rio de Janeiro, Brazil), vol. 58, pp. 21-28.
  • Ferrington Junior, L.C., 2008. Global diversity of non-biting midges (Chironomidae; Insecta-Diptera) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 447-455. http://dx.doi.org/10.1007/s10750-007-9130-1.
    » http://dx.doi.org/10.1007/s10750-007-9130-1
  • Forró, L., Korovchinsky, N.M., Kotov, A.A. and Petrusek, A., 2008. Global diversity of cladocerans (Cladocera; Crustacea) in freshwater. Hydrobiologia, vol. 595, no. 1, pp. 177-184. http://dx.doi.org/10.1007/s10750-007-9013-5.
    » http://dx.doi.org/10.1007/s10750-007-9013-5
  • Fowler, R.T. and Death, R.G., 2001. The effect of environmental stability on hyporheic community structure. Hydrobiologia, vol. 445, no. 1/3, pp. 85-95. http://dx.doi.org/10.1023/A:1017507404733.
    » http://dx.doi.org/10.1023/A:1017507404733
  • Franken, R.J.M., Storey, R.G. and Williams, D.D., 2001. Biological, chemical and physical characteristics of downwelling and upwelling zones in the hyporheic zone of a north-temperate stream. Hydrobiologia, vol. 444, no. 1/3, pp. 183-195. http://dx.doi.org/10.1023/A:1017598005228.
    » http://dx.doi.org/10.1023/A:1017598005228
  • Galassi, D.M.P., 2001. Groundwater copepods (Crustacea: Copepoda): diversity patterns over ecological and evolutionary scales. Hydrobiologia, vol. 453/454, pp. 227-253. http://dx.doi.org/10.1023/A:1013100924948.
    » http://dx.doi.org/10.1023/A:1013100924948
  • Galassi, D.M.P., Huys, R. and Reid, J.W., 2009. Diversity, ecology and evolution of groundwater copepods. Freshwater Biology, vol. 54, no. 4, pp. 691-708. http://dx.doi.org/10.1111/j.1365-2427.2009.02185.x.
    » http://dx.doi.org/10.1111/j.1365-2427.2009.02185.x
  • Gibert, J., STANFORD, J.A., DOLE-OLIVIER, M.-J. and WARD, J.W., 1994. Basic attributes of groundwater ecosystems and prospects for research. In: J. GIBERT, D.L. DANIELOPOL and J.A. STANFORD, eds. Groundwater ecology. San Diego: Academic Press, pp. 7-40.
  • Godbout, L. and Hynes, H.B.N., 1982. The three dimensional distribution of the fauna in a single riffle in a stream in Ontario. Hydrobiologia, vol. 97, no. 1, pp. 87-96. http://dx.doi.org/10.1007/BF00014962.
    » http://dx.doi.org/10.1007/BF00014962
  • Hancock, P.J., Boulton, A.J. and Humphreys, W.F., 2005. Aquifers and hyporheic zones: towards an ecological understanding of groundwater. Hydrogeology Journal, vol. 13, no. 1, pp. 98-111. http://dx.doi.org/10.1007/s10040-004-0421-6.
    » http://dx.doi.org/10.1007/s10040-004-0421-6
  • Harvey, J.W. and Wagner, B.J., 2000. Quantifying hydrologic interactions between streams and their subsurface hyporheic zones. In: J.B. JONES and P.J. MULHOLLAND, eds. Streams and ground waters. San Diego: Academic Press. pp. 3-44.
  • Hunt, G.W. and Stanley, E.H., 2003. Environmental factors influencing the composition and distribution of the hyporheic in Oklahoma streams: variation across ecoregions. Archiv für Hydrobiologie, vol. 158, no. 1, pp. 1-24. http://dx.doi.org/10.1127/0003-9136/2003/0158-0001.
    » http://dx.doi.org/10.1127/0003-9136/2003/0158-0001
  • Hynes, J.D., 1975. Annual cycles of macroinvertebrates of a river in southern Ghana. Freshwater Biology, vol. 5, no. 1, pp. 71-83. http://dx.doi.org/10.1111/j.1365-2427.1975.tb00122.x.
    » http://dx.doi.org/10.1111/j.1365-2427.1975.tb00122.x
  • Iepure, S., Martinez-Hernandez, V., Herrera, S., Rasines-Ladero, R. and De Bustamante, I., 2013. Response of microcrustacean communities from the surface-groundwater interface to water contamination in urban river system of the Jarama basin (central Spain). Environmental Science and Pollution Research International, vol. 20, no. 8, pp. 5813-5826. http://dx.doi.org/10.1007/s11356-013-1529-9. PMid:23475443.
    » http://dx.doi.org/10.1007/s11356-013-1529-9
  • James, A.B.W. and Suren, A.M., 2009. The response of invertebrates to a gradient of flow reduction: an instream channel study in a New Zealand lowland river. Freshwater Biology, vol. 54, no. 11, pp. 2225-2242. http://dx.doi.org/10.1111/j.1365-2427.2009.02254.x.
    » http://dx.doi.org/10.1111/j.1365-2427.2009.02254.x
  • Jones JUNIOR, J.B. and Holmes, R.M., 1996. Surface subsurface interactions in stream ecosystems. Trends in Ecology & Evolution, vol. 11, no. 6, pp. 239-242. http://dx.doi.org/10.1016/0169-5347(96)10013-6. PMid:21237825.
    » http://dx.doi.org/10.1016/0169-5347(96)10013-6
  • Kibichii, S., Baars, J. and Kelly-Quinn, M., 2009. Optimising sample volume and replicates using the Bou-Rouch method for the rapid assessment of hyporheic fauna. Marine & Freshwater Research, vol. 60, no. 1, pp. 83-96. http://dx.doi.org/10.1071/MF08172.
    » http://dx.doi.org/10.1071/MF08172
  • Lafont, M. and Vivier, A., 2006. Oligochaete assemblages in the hyporheic zone and coarse surface sediments: their importance for understanding of ecological functioning of watercourses. Hydrobiologia, vol. 564, no. 1, pp. 171-181. http://dx.doi.org/10.1007/s10750-005-1717-9.
    » http://dx.doi.org/10.1007/s10750-005-1717-9
  • Lee, D.R. and Cherry, J.A., 1978. A field exercise on groundwater flow using seepage meters and mini-piezometers. Journal of Geological Education, vol. 27, pp. 6-10.
  • Lencioni, V., 2004. Survival strategies of freshwater insects in cold environments. Journal of Limnology, vol. 63, no. 1s, pp. 45-55. http://dx.doi.org/10.4081/jlimnol.2004.s1.45.
    » http://dx.doi.org/10.4081/jlimnol.2004.s1.45
  • Lencioni, V., Marziali, L. and Rossaro, B., 2008. Hyporheic chironomids in alpine streams. Boletim do Museu Municipal do Funchal, vol. 13, pp. 127-132.
  • Marchetti, Z.Y. and Carrillo-Rivera, J.J., 2013. Tracing groundwater discharge in the floodplain of the parana river, argentina: implications for its biological communities. River Research and Applications, http://dx.doi.org/10.1002/rra.2629.
    » http://dx.doi.org/10.1002/rra.2629
  • Marmonier, P., Dole-Olivier, M.J. and Creuze Des Châtelliers, M., 1992. Spatial distribution of interstitial assemblages in the floodplain of the Rhône River. Regulated Rivers: Research and Management, vol. 7, no. 1, pp. 75-82. http://dx.doi.org/10.1002/rrr.3450070110.
    » http://dx.doi.org/10.1002/rrr.3450070110
  • Mary, N. and Marmonier, P., 2000. First survey of interstitial fauna in New Caledonian rivers: influence of geological and geomorphological characteristics. Hydrobiologia, vol. 418, no. 1, pp. 199-208. http://dx.doi.org/10.1023/A:1003938629671.
    » http://dx.doi.org/10.1023/A:1003938629671
  • Matthaei, C.D., Arbuckle, C.J. and Townsend, C.R., 2000. Stable surface stones as refugia for invertebrates during disturbance in a New Zealand stream. Journal of the North American Benthological Society, vol. 19, no. 1, pp. 82-93. http://dx.doi.org/10.2307/1468283.
    » http://dx.doi.org/10.2307/1468283
  • Mattos, C.C.L.V., Mattos, M.D.L.V. and Laroche, R.C., 1976. Aspectos do clima e da flora do Parque Nacional do Tijuca. Brasil Flor, vol. 7, pp. 3-12.
  • Medina, H.L., De. Marín, J.C., Gutiérrez, E. and Morales, J., 2003. Nitrogen mobility at the sediment-water interface of Lake Maracaibo, Venezuela. Water, Air, and Soil Pollution, vol. 145, no. 1-4, pp. 341-357. http://dx.doi.org/10.1023/A:1023632702886.
    » http://dx.doi.org/10.1023/A:1023632702886
  • Mori, N. and Brancelj, A., 2011. Spatial and temporal variability of hyporheic invertebrate community within a stream reach of the River Bača (W Slovenia). Natura Sloveniae, vol. 13, no. 1, pp. 25-38.
  • Olsen, D.A. and Townsend, C.R., 2003. Hyporheic community composition in a gravel-bed stream: influence of vertical hydrological exchange, sediment structure and physiochemistry. Freshwater Biology, vol. 48, no. 8, pp. 1363-1378. http://dx.doi.org/10.1046/j.1365-2427.2003.01097.x.
    » http://dx.doi.org/10.1046/j.1365-2427.2003.01097.x
  • Olsen, D.A., Townsend, C.R. and Matthaei, C.D., 2001. Influence of reach geomorphology on hyporheic communities in a gravel ‐ bed stream. New Zealand Journal of Marine and Freshwater Research, vol. 35, no. 1, pp. 181-190. http://dx.doi.org/10.1080/00288330.2001.9516988.
    » http://dx.doi.org/10.1080/00288330.2001.9516988
  • Omesová, M. and Helešic, J., 2007. Vertical Distribution of Invertebrates in Bed Sediments of a Gravel Stream in the Czech Republic. International Review of Hydrobiology, vol. 92, no. 4-5, pp. 480-490. http://dx.doi.org/10.1002/iroh.200610990.
    » http://dx.doi.org/10.1002/iroh.200610990
  • Omesová, M., Horsák, M. and Helešic, J., 2008. Nested patterns in hyporheic meta-communities : the role of body morphology and penetrability of sediment. Naturwissenschaften, vol. 95, no. 10, pp. 917-926. http://dx.doi.org/10.1007/s00114-008-0399-3. PMid:18542903.
    » http://dx.doi.org/10.1007/s00114-008-0399-3
  • Orghidan, T., 1959. Ein neuer Lebensraum des unterirdischen Wasser: der hyporheische Biotop. Archiv für Hydrobiologie, vol. 55, pp. 392-414.
  • Pinder, L.C.V., 1986. Biology of freshwater chironomidae. Annual Review of Entomology, vol. 31, no. 1, pp. 1-23. http://dx.doi.org/10.1146/annurev.en.31.010186.000245.
    » http://dx.doi.org/10.1146/annurev.en.31.010186.000245
  • R DEVELOPMENT CORE TEAM, 2013. R: A language and environment for statistical computing. Version 2.15.0 [software]. Vienna: R Foundation for Statistical Computing.
  • Resh, H.R. and Rosenberg, D.M., 1984. The ecology of aquatic insects. New York: Praeger Publishers. 625 p.
  • Robertson, A.L., Lancaster, J. and Hildrew, A.G., 1995. Stream hydraulics and the distribution of microcrustacea: A role for refugia? Freshwater Biology, vol. 33, no. 3, pp. 469-484. http://dx.doi.org/10.1111/j.1365-2427.1995.tb00407.x.
    » http://dx.doi.org/10.1111/j.1365-2427.1995.tb00407.x
  • Romero-González, M.E., Zambrano, E., Mesa, J. and Medina, H.L., 2001. Fractional phosphate composition in sediments from a tropical river (Catatumbo River, Venezuela). Hydrobiologia, vol. 450, no. 1-3, pp. 47-55. http://dx.doi.org/10.1023/A:1017535216608.
    » http://dx.doi.org/10.1023/A:1017535216608
  • Schwoerbel, J., 1967. Das hyporheische Interstitial als Grenzbiotop zwischen oberirdischem und subterranem Ökosystem und seine Bedeutung für die Primär-Evolution von Kleinsthöhlenbewohnern. Archiv für Hydrobiologie, vol. 33, no. 6, pp. 1-62.
  • Sedell, J.R., Reeves, G.H., Hauer, F.R., Stanford, J.A. and Hawkins, C.P., 1990. Role of refugia in recovery from disturbances: modern fragmented and disconnected river systems. Environmental Management, vol. 14, no. 5, pp. 711-724. http://dx.doi.org/10.1007/BF02394720.
    » http://dx.doi.org/10.1007/BF02394720
  • Smith, I.M. and COOK, D.R. 1991. Water mites. In: J.H. THORP and A.P. COVICH, eds. Ecology and classification of North American freshwater invertebrates. San Diego: Academic Press, pp. 523-592.
  • Stanford, J.Á. and Ward, J.V., 1988. The hyporheic habitat of river ecosystem. Nature, vol. 335, no. 6185, pp. 64-66. http://dx.doi.org/10.1038/335064a0.
    » http://dx.doi.org/10.1038/335064a0
  • Strahler, A.N., 1957. Quantitative analysis of watershed geomorphology. T. American Geophysical Union, vol. 38, no. 6, pp. 913-920. http://dx.doi.org/10.1029/TR038i006p00913.
    » http://dx.doi.org/10.1029/TR038i006p00913
  • Stubbington, R., 2012. The hyporheic zone as an invertebrate refuge: a review of variability in space, time, taxa and behavior. Marine & Freshwater Research, vol. 63, no. 4, pp. 293-311. http://dx.doi.org/10.1071/MF11196.
    » http://dx.doi.org/10.1071/MF11196
  • Thibodeaux, L.J. and Boyle, J.D., 1987. Bedform-generated convective transport in bottom sediment. Nature, vol. 325, no. 6102, pp. 341-343. http://dx.doi.org/10.1038/325341a0.
    » http://dx.doi.org/10.1038/325341a0
  • Valett, H.M., 1993. Surface-hyporheic interactions in a Sonoran Desert stream: hydrologic exchange and diel periodicity. Hydrobiologia, vol. 259, no. 3, pp. 133-144. http://dx.doi.org/10.1007/BF00006593.
    » http://dx.doi.org/10.1007/BF00006593
  • Van Damme, K., Brancelj, A. and Dumont, H.J., 2009. Adaptations to the hyporheic in Aloninae (Crustacea: Cladocera): allocation of Alona protzi Hartwig, 1900 and related species to Phreatalona gen. nov. Hydrobiologia, vol. 618, no. 1, pp. 1-34. http://dx.doi.org/10.1007/s10750-008-9607-6.
    » http://dx.doi.org/10.1007/s10750-008-9607-6
  • Vigna Taglianti, A., Cottarelli, V. and Argano, R., 1969. Messa a punto di metodiche per la raccolta della fauna interstiziale e freatica. Archivio Botanico e Biogeografico Italiano, vol. 45, no. 14, pp. 375-380.
  • Williams, D.D. and Hynes, H.B.N., 1974. The occurrence of benthos deep in the substratum of a stream. Freshwater Biology, vol. 4, no. 3, pp. 233-256. http://dx.doi.org/10.1111/j.1365-2427.1974.tb00094.x.
    » http://dx.doi.org/10.1111/j.1365-2427.1974.tb00094.x

Publication Dates

  • Publication in this collection
    Nov 2015

History

  • Received
    13 Nov 2013
  • Accepted
    17 Apr 2014
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
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