Fish As Ecological Tools to Complement Biodiversity Inventories of Benthic Macroinvertebrates
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Hydrobiologia DOI 10.1007/s10750-011-0747-8 PRIMARY RESEARCH PAPER Fish as ecological tools to complement biodiversity inventories of benthic macroinvertebrates Daniel M. Maroneze • Taynan H. Tupinamba´s • Carlos B. M. Alves • Fa´bio Vieira • Paulo S. Pompeu • Marcos Callisto Received: 3 October 2010 / Revised: 2 May 2011 / Accepted: 4 May 2011 Ó Springer Science+Business Media B.V. 2011 Abstract Sampling benthic macroinvertebrates in macroinvertebrates as a food resource for fishes, the large rivers has several limitations, arising not sampling restrictions in sediment collection done by only from the selectivity of traditional sampling dredges, and the importance of surveying benthos gears but also from difficulty in capturing organisms biodiversity, the objective of this study was to that inhabit the deeper zones and high current evaluate the stomach contents of five commonly- velocities. Considering the importance of benthic occurring invertivorous fish species as a means of complementing a benthic macroinvertebrate inven- tory. Three sampling campaigns (fish and benthic Handling editor: Luiz Carlos Gomes macroinvertebrate) were conducted in a reach of the Electronic supplementary material The online version of Araguari River (Minas Gerais, Brazil), approximately this article (doi:10.1007/s10750-011-0747-8) contains 9 km long and 90 m wide. Astyanax altiparanae supplementary material, which is available to authorized users. Garutti & Britski 2000, Leporinus friderici (Bloch 1794), Leporinus amblyrhynchus Garavello & Britski D. M. Maroneze Á T. H. Tupinamba´s Á M. Callisto (&) Laborato´rio de Ecologia de Bentos, Departamento de 1987, Iheringichthys labrosus (Lu¨tken 1874) and Biologia Geral, Instituto de Cieˆncias Biolo´gicas, Pimelodus maculatus Lacepe`de 1803 were the fish Universidade Federal de Minas Gerais, species collected and studied. To determine benthic Av. Antoˆnio Carlos, 6627, C.P. 486, Pampulha, macroinvertebrate taxonomic richness, a total of 54 CEP 30161-970 Belo Horizonte, MG, Brazil e-mail: [email protected] Van Veen sediment samples were obtained. We URL: http://www.biogeral.icb.ufmg.br/benthos compared lists of the benthic taxa found in fish stomachs with those from the sediment samples. C. B. M. Alves Á P. S. Pompeu Á M. Callisto The differences in the taxonomic composition of the Nuvelhas/Projeto Manuelza˜o, Universidade Federal de Minas Gerais, Av. Antoˆnio Carlos, 6627, Pampulha, benthic macroinvertebrate communities between the CEP 31270-901 Belo Horizonte, MG, Brazil sediment samples and each fish species stomachs contents were assessed through NMDS and ANOSIM F. Vieira analyses, using a Sorensen similarity index with the Centro de Transposic¸a˜o de Peixes, Universidade Federal de Minas Gerais, Ageˆncia Shopping Del Rey, C. P. 4011, presence/absence of taxa data. Independent of sam- CEP 31250-970 Belo Horizonte, MG, Brazil pling period, additional benthic macroinvertebrate families or classes were provided by identifying fish P. S. Pompeu stomach contents. We found a total of 30 taxa in this Departamento de Biologia, Universidade Federal de Lavras, Campus Universita´rio, CEP 37200-000 Lavras, study, including 5 unique taxa (or 17% of the total) in MG, Brazil the sediment samples, 9 unique taxa (30%) in the 123 Hydrobiologia stomach samples, and 16 taxa (53%) common to condition at a site (Junqueira et al., 2000; Karr & both. The NMDS and ANOSIM analyses showed a Chu, 2000; Buss & Borges, 2008) or for taxonomic significant separation between Van Veen sediment inventories that seek to provide a list of common samples and two fish species stomach contents— species in a specific area (Mackey et al., 1984). L. amblyrhynchus and P. maculatus. These results Recent studies have shown that analysis of stomach indicate that fish can be used as additional samplers contents of benthophagous fishes can be an important and are an efficient method to complement the strategy in taxonomic surveys (Russo et al., 2002; benthic taxonomic inventory obtained through tradi- Tupinamba´s et al., 2007; Santos et al., 2009) because tional sediment sampling techniques in large areas, as fish exploit a wide variety of microhabitats and river segments and catchments. capture macroinvertebrates in areas that are difficult to sample with conventional gears. Their feeding Keywords Stomach contents Á Samplers Á behaviors may make fish useful complementary Benthos Á Large rivers Á Trophic interactions benthos samplers (Callisto et al., 2002; Galina & Hahn, 2004). To evaluate the importance of fish stomach Introduction analyses for taxonomic inventories of benthic macr- oinvertebrate communities, we analyzed stomach Benthic macroinvertebrate sampling techniques are contents of five common invertivorous species highly varied. In each type of aquatic habitat, differing (Dura˜es et al., 2001; Callisto et al., 2002): Astyanax methods are used because of differing depths, sediment altiparanae Garutti & Britski 2000, Leporinus frid- textures, currents, and spatial heterogeneities of the area erici (Bloch 1794), Leporinus amblyrhynchus Garav- (Alves & Strixino, 2003; Blockson & Flotemersch, ello & Britski 1987, Iheringichthys labrosus (Lu¨tken 2005; Kikuchi et al., 2006). In large rivers, Surber 1874) and Pimelodus maculatus Lacepe`de 1803. We samplers or dredges (i.e., Eckman-Birge, Van Veen, hypothesized that benthic macroinvertebrate families Petersen, etc.) are commonly used (Bournaud et al., and classes (operational taxonomic units, OTU) 1998; Rempel et al., 2000; Gayraud et al., 2003;Moreno found in fish stomachs would differ from those found et al., 2009), and because the sampling area is known, in sediment samples because of fish foraging strate- such methods aid quantitative analysis of benthic gies. In addition, we evaluated whether fish stomach- macroinvertebrate communities (Bady et al., 2005). content analysis could effectively complement taxo- Comprehensive quantitative samples require nomic surveys conducted with conventional benthos substantial time and funds to obtain and identify sampling gears. (Rosenberg et al., 1997; Bartsch et al., 1998). Also, such samples are performed in specific habitats and as a consequence, some of the benthos unique to other Materials and methods habitats are not adequately sampled (Lenat, 1988). These limitations often occur in large rivers where We conducted the study in a reach of the Araguari sampling of benthic macroinvertebrates is concen- River (Brazil) between 18°200S–46°000W and trated in shallow areas near river margins (Reece & 20°10’S–48°50’W. The reach was 9 km long and Richardson, 2000). Sampling in the deeper zones or approximately 90 m wide, drains mainly sandstone areas of strong current normally is not conducted and basalt lithology, and in its deepest valley erodes because of access and safety concerns for the sampling granite and gneiss (Rodrigues, 2002). The local crew, and the need to use equipment such as suction climate is characterized by a rainy period from pumps and SCUBA divers (Rosenberg et al., 1997)or October to March and a dry period from May to artificial substrates that require multiple site visits September. The average annual temperature is 22°C (Humphries et al., 1998; Collier et al., 2009). with a total rainfall of 1,555 mm/year (Rosa et al., Depending on the purpose of the research, qual- 2006). In general, the river water is well oxygenated, itative samples are sufficient. This is the case for slightly acidic, and low in electrical conductivity, water quality biomonitoring programs that convert turbidity, and total dissolved nutrients (Maroneze data to a biotic index score to determine assemblage et al., 2011). 123 Hydrobiologia We sampled in July 2005, October 2005, and June We used the same procedure to evaluate and identify 2008 at six sites along the 9-km reach averaging the organisms present in fish stomach contents. We 1.5 km apart. Fishes were caught in 10 m 9 1.7 m compared lists of the benthic OTU found in fish gill nets with mesh sizes 3, 4, 5, 6, 7, 8, 10, 12, 14, stomachs with those from the sediment samples. To and 16 cm between opposite knots. At each site, we eliminate the influence of the unequal number of fished a total of 170 m2 of gill nets from dusk to the stomachs analyzed and to determine which fish following morning for approximately 14 h. The species contributed most to the inventory, we also collected fish were fixed with 10% formalin. In the calculated the average number of exclusive taxa per laboratory, the fish were soaked in water, transferred stomach (NT) through use of the following formula: o nx to alcohol 70 GL, identified, weighed, and measured. NT ¼ Nx, where nx is the number of taxa found in the The number of stomachs removed and evaluated stomach contents of species x and not found in the varied between species, size, and month (Table 1). sediment samples, and Nx is the number of stomachs The standard length (cm) of the smallest sampled fish of species x analyzed. The greater the value of NT, in advanced maturation was used to separate the the greater the contribution of that fish species toward juveniles from adults (Vono et al., 2002; Froese & adding benthic OTU to the inventory. Pauly, 2010). Empty stomachs were excluded from The differences in the taxonomic composition of analysis. the benthic macroinvertebrate communities between To evaluate the composition of benthic macroin- the sediment samples and each fish species stomachs vertebrate communities, we took three Van Veen contents were assessed through a non-metric dimen- (0.45 m2) sediment samples from the river margins in sional scaling (NMDS) ordination technique, using a each of the fish sampling stations. The material was Sorensen similarity index with the presence/absence only collected along the margins because of the rocky of taxa data. The statistical significance of the group- nature of the central axis of the river. A total of 54 ings (sediment samples vs. fish stomachs contents) Van Veen sample units were obtained (6 sites 9 3 were tested through similarity analysis (ANOSIM) samples/site 9 3 visits/site). In the laboratory, we (a = 0.05).