Can organic and conventional agricultural systems affect wetland macroinvertebrate taxa in rice fields?

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Abstract

The use of agrochemicals, water management and intense mechanization is compromising species diversity in rice fields. Organic agriculture has been proposed as a way to reduce the pressure on biodiversity in agricultural landscapes. Therefore, the following hypotheses were tested: (1) Taxonomic richness and abundance of macroinvertebrates are lower in rice fields than in natural ponds; (2) Conventional rice crops decrease taxonomic richness and abundance of macroinvertebrates compared with organic crops; (3) Taxonomic macroinvertebrate composition in organic rice crops is more similar to the composition in natural ponds than conventional fields; and (4) A reduction of taxonomic richness, abundance as well as a modified composition during soil preparation and the initial growth phases of the rice cultivating cycle were expected. To test these hypotheses, four natural ponds, four organic and four conventional rice fields were selected in southern Brazil. In each area, six collections were carried out over the rice cultivation cycle (August 2010 to August 2011). A total of 25,449 individuals from 73 different taxa were sampled. The richness and abundance were higher in ponds than in rice crops in the anterior and posterior off-season and in the soil preparation periods. However, organic and conventional rice fields showed similar taxonomic richness and abundance. Although the taxonomic composition differed only between rice crops and ponds, the presence of many taxa that only occur in organic crops and ponds indicates that organic management favors the establishment of some pond macroinvertebrate taxa in rice agroecosystems, mainly predators. Our results should be seen as an incentive for more sustainable production with less impact on the environment.

Zusammenfassung

Der Einsatz von Agrochemikalien, Bewässerungsmanagement und intensive Mechanisierung beeinträchtigen die Artendiversität in Reisfeldern. Biologische Landwirtschaft wurde als eine Möglichkeit vorgeschlagen, den Druck auf die Biodiversität in der Agrarlandschaft zu mindern. Wir überprüften deshalb die folgenden Hypothesen: (1) Taxonomische Diversität und die Abundanz von Makroinvertebraten sind auf Reisfeldern geringer als in natürlichen Tümpeln. (2) Konventioneller Reisanbau verringert die Anzahl der Taxa und die Abundanz der Makroinvertebraten im Vergleich zu biologischem Anbau. (3) Die taxonomische Zusammensetzung der Makroinvertebraten auf biologischen Reisfeldern ähnelt der von natürlichen Tümpeln stärker als der von konventionellen Feldern. (4) Eine Reduktion der Taxonzahlen, Abundanz sowie eine veränderte Zusammensetzung wurden für die Zeit der Feldvorbereitung und die frühen Wachstumsphasen erwartet. Wir untersuchten jeweils vier natürliche Tümpel sowie biologische und konventionelle Reisfelder in Süd-Brasilien. An jedem Standort wurden sechs Probenahmen im Laufe des Reis-Anbauzyklus’ durchgeführt (August 2010 bis August 2011). Insgesamt wurden 25,449 Individuen aus 73 Taxa gesammelt. Während der Ruhephase vor und nach dem Anbau sowie während der Bodenvorbereitungsphase waren taxonomische Diversität und Abundanz in den Tümpeln höher als auf den Reisfeldern. Biologische und konventionelle Reisfelder zeigten ähnliche taxonomische Diversität und Abundanz. Auch wenn die taxonomische Zusammensetzung sich nur zwischen Tümpeln und Reisfeldern unterschied, zeigte das Auftreten von Taxa, die nur in Tümpeln und auf biologischen Feldern nachgewiesen wurden, dass biologische Bewirtschaftung die Ansiedlung von einigen Tümpel bewohnenden Makroinvertebraten (hauptsächlich Prädatoren) auf Reisfeldern begünstigt. Unsere Ergebnisse sollten als ein Anreiz zu mehr nachhaltiger Produktion mit weniger Auswirkungen auf die Umwelt gesehen werden.

Introduction

Wetlands are priority ecosystems for conservation due to their vast biological diversity and productivity. Despite their importance, wetlands are amongst the most affected and degraded ecological systems (RAMSAR 2013). Almost half of the world's wetlands disappeared in the last century (Shine & Klemm 1999).Agricultural expansion is one of the main human activities responsible for the decline of natural wetlands throughout the world, with severe consequences for species conservation (Benton, Vickery, & Wilson 2003; Fuller et al. 2005).

Rice field expansion is one of the main human activities responsible for the decline of natural wetlands throughout the world (Russi et al. 2013). Rice is grown in over 100 countries today over the world (Juliano 1993), and currently 165 million hectares are occupied by rice fields. Asia accounts for 89% of that (FAO 2013). Brazil, the ninth-largest rice producer on earth, has a cultivated area of 2.5 million hectares and production of 12.5 million tons/year (USDA 2013).

Rice fields have been defined as man-made wetlands by the Ramsar Convention for grain produce (RAMSAR 2013). Some characteristics of rice fields, such as periodic flooding, make them similar to intermittent wetlands (Bambaradeniya et al., 2004, Lupi et al., 2013). Rice fields help to maintain regional biodiversity of many vertebrate and invertebrate species, and they act as supplemental habitats for many species of aquatic plants, invertebrates, amphibians and birds throughout the world (Elphick, 2010, Piatti and Souza, 2011; Lupi et al., 2013, Rizo-Patrón et al., 2013; Zhang et al. 2013), including southern Brazil (Stenert, Bacca, Maltchik, & Rocha 2009; Machado & Maltchik 2010; Rolon & Maltchik 2010; Guadagnin, Peter, Rolon, Stenert, & Maltchik 2012). An important question in terms of biodiversity conservation is to know whether agricultural wetlands can maintain high levels of biodiversity and help species conservation. The development of new management practices which reconcile the sustainability of rice fields and the conservation of species could help to maintain a rich biodiversity outside protected areas.

Southern Brazil rice fields are cultivated under different systems, which differ in the use of agrochemicals, water management and mechanization. Conventional systems involve intense mechanization and the irrigation water contains pesticides and chemical fertilizers. Organic systems do not utilize agrochemicals and instead use animal manure and plant debris as fertilizers. These organic systems also use elaborate crop rotation techniques, including the use of nitrogen-fixing plants and water level management to control weeds (Andersson, Rundlöf, & Smith 2012). Organic agriculture has been proposed as a way to reduce the pressure placed on biodiversity in the agricultural landscape (Brittain, Bommarco, Vighi, Settele, & Potts 2010; Andersson et al. 2012). Several studies have shown that organic farming enhances biodiversity more than conventional farms (Bengtsson, Ahnstrom, & Weibull 2005Fuller et al., 2005, Hole et al., 2005).

Aquatic macroinvertebrates are the most diverse and abundant organisms in wetlands, providing food for several wildlife species and they have been used to monitor water quality of aquatic ecosystems (Resh, 2007, Melo et al., 2015). In rice fields, macroinvertebrates have a beneficial role for soil fertility because they significantly contribute to the nutrient cycling, and they include predators and parasitoids essential for the natural control of rice pests and vectors of human and animal diseases (Roger, Heong, & Teng 1991).

Some studies in southern Brazil identified environmental predictors of diversity patterns and community structure of aquatic macroinvertebrates in wetlands (Stenert et al., 2008, Maltchik et al., 2012; Crippa, Stenert, & Maltchik 2013) and rice fields (Stenert et al., 2009, Maltchik et al., 2011; Stenert, Maltchik, & Rocha 2012). However, few studies have focused on differences between conventional and organic rice crops (Wilson, Watts, & Stevens 2008; Rizo-Patrón et al. 2013). Direct exposure to herbicides, insecticides and chemical fertilizers can affect macroinvertebrate diversity by reducing richness, changing composition and increasing dominance of common species (Leitão, Pinto, Pereira, & Brito 2007Wilson et al., 2008, Rizo-Patrón et al., 2013). Moreover, soil tillage caused by intense mechanization and hydric stress from hydrological fluctuations impair the establishment of late-successional and long-lived species (Suhling et al., 2000, Bambaradeniya et al., 2004). Recently, Dalzochio, Baldin, Stenert, and Maltchik (2015) showed that organic rice fields favored some functional traits of aquatic insects, like the presence of genera sensitive to pesticides, more active and predatory insects, and fewer generations per year, when compared to conventional farming in southern Brazil.

Assuming that aquatic macroinvertebrate taxonomic richness, abundance and composition are strongly influenced by the adopted agricultural practices in rice fields, such as water level control, agrochemical application and machinery usage, and that the application of pesticides may cause mortality of some taxa, leading to larger populations of some dominant and resilient species (Roger et al., 1991, Wilson et al., 2008, Rizo-Patrón et al., 2013), the following hypotheses were tested: (1) Taxonomic richness and abundance of macroinvertebrates are lower in rice fields than in natural ponds; (2) Conventional rice crops decrease macroinvertebrate taxonomic richness and abundance compared with organic crops; (3) Taxonomic macroinvertebrate composition in organic rice crops is more similar to the composition in natural ponds than conventional fields. Furthermore, assuming that the absence of water during tillage suppressed the occurrence and abundance of some aquatic macroinvertebrate taxa with low tolerance to drought (Williams 1996), a reduction of taxonomic richness, abundance as well as a modified composition during soil preparation and the initial growth phases of the rice cultivating cycle are expected.

Section snippets

Study area

Rio Grande do Sul is the southernmost state in Brazil, with an area of approximately 282,000 km2. The coastal plain in southern Brazil concentrates one of the highest densities and diversities of wetlands in southern Brazil (Maltchik, Schneider, Becker, & Escobar 2003). The climate is subtropical humid and the average annual temperature is 17.5 °C, ranging between 4.6 °C in winter and 22.2 °C in summer. The rainfall averages 1250 mm/yr and ranges from 1150 to 1450 mm/yr. Although there have been

Data analysis

Macroinvertebrate taxonomic richness and abundance corresponded to the number of taxa and individuals, respectively. Differences in macroinvertebrate richness and abundance between rice crops (organic and conventional) and natural ponds over time were tested using Repeated Measures Analysis of Variance (ANOVA), performed using SPSS software, version 17.0 (Polar Engineering and Consulting, Nikiski, U.S.A.) (SPSS Inc 2008). Tukey tests were applied for multiple comparisons of the taxonomic

Results

A total of 25,449 individuals from 73 different taxa (orders, families and genera) were collected during the rice cultivation cycle (see Appendix A: Table 2). Insecta was the most abundant class (n = 15,626), followed by Oligochaeta (n = 7017) and Hirudinea (n = 1734). The most abundant family was Chironomidae (n = 5952), followed by Libellulidae (n = 1294) and Corixidae (n = 1232). Most families were represented by only one genus (see Appendix A: Table 2).

A total of 16,487 individuals from 70 different

Discussion

Chironomidae was the most abundant taxon in organic and conventional rice crops, followed by oligochaetes and leeches. The predominance of chironomid larvae in our study was also verified in Philippine rice fields, with about 8000 to 10,000 individuals/m2 (Simpson, Roger, Oficial, & Grant 1994). Populations of larvae up to 18,000 individuals/m2, corresponding to seven genera, were recorded in California rice fields (Clement, Grigarick, & Way 1977). Chironomids were reported to be the most

Conclusions

This study indicates that rice fields are used as a complementary habitat by aquatic macroinvertebrate communities in southern Brazil. Although our study showed similar macroinvertebrate responses between organic and conventional rice fields, some taxa, mainly predators, only occur in organic crops and natural ponds. Macroinvertebrate predators in rice fields have a beneficial role for the control of rice pests and vectors of human and animal diseases (Roger et al. 1991). In this sense, organic

Acknowledgements

This research was supported by funds from Universidade do Vale do Rio dos Sinos - UNISINOS (02.00.023/00-0), Conselho Nacional de Desenvolvimento Cientifico e Tecnologico - CNPq (140101/2010-1) and FAPERGS (11/1149-7). Leonardo Maltchik holds a Brazilian Research Council - CNPq Research Productivity grant. We declare that the data collection complied with the Brazilian current laws.

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