AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 39–46 (2010) Published online 28 September 2009 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/aqc.1070
Can management practices in rice fields contribute to amphibian conservation in southern Brazilian wetlands? IBEREˆ FARINA MACHADO and LEONARDO MALTCHIK Laboratory Ecology and Conservation of Aquatic Ecosystems, Universidade do Vale do Rio dos Sinos, UNISINOS. Av. Unisinos, no. 950, CEP 93.022-000.Sa˜o Leopoldo, Rio Grande do Sul, Brazil ABSTRACT 1. Rice field expansion is one of the activities associated with the disappearance of 90% of the wetlands in southern Brazil. Worldwide, rice agriculture has been recognized as having considerable potential value for many aquatic species. Nevertheless, management practices in such systems must be ameliorated and better investigated. 2. This study evaluated the potential role of rice fields as refugia for amphibians, and whether different hydrologic management practices after rice cultivation could contribute to wetland amphibian conservation in southern Brazil. 3. Six collections were made in six rice fields with different management practices after cultivation (three dry and three flooded) and three natural wetlands. The amphibians were sampled through six random 15-min visual transects per collection in each rice field and the natural wetlands. 4. In total, 2139 anuran individuals were observed in rice fields (798) and Reserva Lake (1341), comprising 12 anuran species distributed among five anuran families. Anuran richness and abundance varied over the rice cultivating cycle, and they were higher in the growing phases than in the fallow phases. The mean anuran richness and abundance was higher in Reserva Lake than in flooded and dry rice fields. 5. The different management practices adopted after the harvesting period (presence or lack of surface water) did not influence the anuran richness and abundance. It did, however, influence species composition. 6. The difference in species composition between the management practices adopted is an interesting result in terms of biodiversity conservation. Rice producers could maintain part of their agricultural land flooded during the fallow phase as a strategy to preserve a higher diversity of anurans. These results should be taken into consideration in wetland conservation plans in southern Brazil; however, the percentage of each agricultural land that should be kept flooded should be decided by Brazilian agricultural and conservation policies. Such a strategy would reconcile agricultural/economic needs with the conservation of biodiversity in southern Brazil, where more than 90% of wetland systems have already been lost. Copyright r 2009 John Wiley & Sons, Ltd. Received 9 January 2009; Revised 10 July 2009; Accepted 30 July 2009 KEY WORDS:
anura; management practices; rice cultivating cycle; Neotropical region
INTRODUCTION Wetlands are important conservation sites because they support rich biodiversity and high productivity (Davis et al., 1996; Getzner, 2002). However, more than 50% of wetlands in parts of North America, Europe, Australia, and New Zealand were converted during the twentieth century (Millennium Ecosystem Assessment, 2005). Agricultural expansion is one of the main human activities responsible for the decline of natural
wetlands throughout the world (Czech and Parsons, 2002). As part of this expansion, rice cultivation (Oryza sativa L.) plays an important role as the most important cereal crop in the developing world (Juliano, 1993). In 2003, approximately 151 million hectares of land were cultivated with rice globally, and Asia accounted for 89% of that (FAO Stat, 2004). Worldwide, rice fields have been recognized as having considerable potential value for many species of aquatic invertebrates, plants, and vertebrates such as fish,
*Correspondence to: L. Maltchik, Laboratory Ecology and Conservation of Aquatic Ecosystems, Universidade do Vale do Rio dos Sinos, UNISINOS, Av. Unisinos, no. 950, CEP 93.022-000.Sa˜o Leopoldo, Rio Grande do Sul, Brazil. E-mail:
[email protected]
Copyright r 2009 John Wiley & Sons, Ltd.
40
I.F. MACHADO AND L. MALTCHIK
amphibians, and birds (Fernando et al., 1979; Miller et al., 1989; Burhanuddin, 1993; Brouder and Hill, 1995; Elphick and Oring, 1998, 2003; Czech and Parsons, 2002; Bambaradeniya and Amarasinghe, 2003). Given that agricultural wetlands, such as rice crops, grow at the expense of natural wetlands, the important question from the point of view of biodiversity conservation is whether these agricultural wetlands can function adequately to maintain high levels of biodiversity. Therefore, the development of new concepts and management practices that reconcile the sustainability of rice fields and the conservation of species will demand greater understanding of these complex agroecosystems. For instance, Californian rice producers usually flood their plantations after harvesting to accelerate straw decomposition. This may be an important strategy for biodiversity conservation, given that such action creates important habitats for waterbird communities (Brouder and Hill, 1995; Elphick and Oring, 2003). Since protected areas cover only 11.5% of the planet’s surface (Rodrigues et al., 2004), rice fields and their large inundated areas may be essential in the conservation of wetland species. One of the main hydrological characteristics of South America is the existence of large wetlands (Neiff, 2001). In southern Brazil, approximately 72% of wetlands are smaller than 1 km2 (Maltchik, 2003). This pattern is a consequence of severe habitat fragmentation due to agricultural expansion, especially rice plantations (Gomes and Magalha˜es, 2004). Conservative estimates indicate that approximately 90% of wetlands have disappeared in southern Brazil. Several studies have analysed biodiversity patterns in fragmented wetlands in southern Brazil (Rolon and Maltchik, 2006; Guadagnin and Maltchik, 2007; Stenert and Maltchik, 2007; Rolon et al., 2008; Stenert et al., 2008), but the role of rice fields as biodiversity refuges in the Neotropics remains poorly known. Such information is extremely important to guide policies for biodiversity conservation, since protected areas correspond to less than 1% of the land in southern Brazil (Brasil, 2006), a number far below the goal of 10% proposed by the Brazilian Ministry of Environment (Ministe´rio do Meio Ambiente Brasileiro–Brasil, 2006). Wetlands serve as important breeding sites for many amphibian species (Moler and Franz, 1987; Dodd, 1992; Semlitsch, 1998), and some anuran species breed only in wetland systems (Dodd and Cade, 1998). The loss of wetland
systems can compromise several anuran species in southern Brazil, including endemic ones (Silvano and Segalla, 2005). In Japan, rice fields are important habitats for many species of anurans at some stage of their life cycles, especially as breeding habitat (Fujioka and Lane, 1997). However, the importance of rice fields to the conservation of amphibian species in the Neotropical region is scarcely studied. This information is extremely important in southern Brazil, given that the region has about 11% of the anuran species identified in Brazil, the country with the largest amphibian diversity in the world (Machado and Maltchik, 2007; SBH, 2009). Irrigated rice fields in southern Brazil present a dynamic hydrologic regime, with variation between aquatic and terrestrial phases, remaining without surface water for 2 years during the fallow phase. The fallow phase represents the period when the agricultural land remains without rice culture. In this phase, the agricultural land is drained. However, some rice fields are kept flooded because they are located in lower arable lands. The objectives of this study were: (1) to analyse the anuran richness, abundance and composition in rice fields over the rice cultivating cycle; (2) to compare the richness, abundance, and composition of anuran amphibians in rice fields with different hydrological management practices (flooded and dry); (3) to compare anuran amphibian richness, abundance, and composition in rice fields with that in natural wetlands.
METHODS Study area The state of Rio Grande do Sul (RS) is located in southern Brazil (271040 –331450 S; 491420 –571380 W) and has an area of 282.184 km2 (Figure 1). The Coastal Plain of Rio Grande do Sul is an important irrigated rice producer in South America (Azambuja et al., 2004). The Coastal Plain is one of the regions in southern Brazil with the highest concentration of wetlands (Maltchik et al., 2003). The climate is humid subtropical and the mean annual temperature is 17.51C. The mean annual rainfall reaches 1250 mm yr1 and ranges between 1150 and 1450 mm yr1 (Tagliani, 1995). The absence of hills and the low altitude (lower than 20 m above sea level) throughout the study area makes the climatic conditions (precipitation and
Figure 1. Study area and rice fields studied, Mostardas municipality, Rio Grande do Sul, Brazil (F 5 flooded fields with retained water during the fallow phase; D 5 dry fields that were dry during the fallow phase; LR 5 Reserva Lake). Copyright r 2009 John Wiley & Sons, Ltd.
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 39–46 (2010) DOI: 10.1002/aqc
MANAGEMENT PRACTICES IN RICE FIELDS AND AMPHIBIAN CONSERVATION
temperature) very similar among the study wetland systems (Rambo, 2000). The study was carried out in Mostardas County (Coastal Plain of Rio Grande do Sul). Mostardas is the eighth largest producer of irrigated rice in southern Brazil, and the rice cropping area covers approximately 33.397 ha (IRGA, 2007). In the rice fields, glyphosate application is ordinarily conducted in two phases: tillage (4 L ha1) and the beginning of rice emergence (2 L ha1). Rice fields are fertilized with urea (200 kg ha1) before irrigation and after rice emergence.
Field sampling Rice fields were categorized as two types according to management practice after harvesting: (1) flooded, representing sites in lower arable lands which are kept flooded; and (2) dry, for sites in the upper lands, which are drained and used for cattle grazing (Figure 1). A set of 20 rice fields with different hydrological management practices was selected (10 flooded and 10 drained), and six were selected randomly — three dry fields and three flooded fields (Figure 1). Each rice field investigated was approximately 1 ha. In each rice field, six collections were carried out over the rice cultivating cycle (June 2005 to June 2006), which comprised the main phases: two collections in the fallow phase (June 2005 and September 2005), one collection during the tillage phase (November 2005), two collections in the rice growing season (rice emergence — January 2006, and tilling — March 2006), and one collection after harvesting (June 2006). The fallow phase represents the period when the agricultural land remains without rice culture, and the tillage phase represents the period when the soil is prepared for planting, including ploughing, herbicide and fertilizer application and sowing. In flooded rice fields, the surface water was present during all phases of the cycle, except in the tillage phase, whereas in the dry rice fields the surface water was present only during the growing season (rice emergence and tilling). Three surveys were conducted within a single large natural wetland remnant (Reserva Lake — area about 9.93 km2), due to the lack of small wetland natural fragments with similar size and hydroperiods of rice fields along the study area. Reserva Lake was chosen for three reasons: it was the natural remnant closest to the study rice fields; it is the only water supply for the rice fields; and the wetland margin drought and the hydroperiod of three natural surveys were similar to the rice fields. Ten sampling sites of 1 ha each were selected along the lake margin (Figure 1), and three were selected randomly. The minimum distance between the sampling sites was 1.5 km to increase the independence of the sampled areas. Six collections were made over the rice cultivating cycle (June 2005 to June 2006). The amphibians were sampled through visual transects between sunset and 01:00. On each occasion, six 15-min transects were sampled in each rice field (three dry and three wet), and in the three sampling sites of Reserva Lake. This amounted to 90 min of sampling at each sampling site. Each transect had its starting point randomized and they were sequentially distributed perpendicular to the length of the rice fields studied and the sampling sites of Reserva Lake. On each sampling occasion, the sequence of the visits was randomized using a table of random numbers. All of the observed Copyright r 2009 John Wiley & Sons, Ltd.
41
individuals were counted and identified according to Cei (1980), Loebmann (2005) and Rosset (2008).
Data analysis The total and mean anuran richness and abundance per sampled area were the cumulative and mean values of species and individuals observed, respectively. Differences in anuran richness and abundance between rice fields (flooded and dry) and Reserva Lake over time (six phases) were tested using repeated measures ANOVA. The analysis was performed using SPSS (2002). In order to reduce heteroscedasticity, anuran abundance was square-root transformed. The Levene’s test verified the homogeneity of variance and Mauchy’s test verified the sphericity assumption. The repeated measures ANOVA approach assumes a compound symmetry (homogeneity of the variance–covariance matrix); the G-G corrections were used for the F test (von Ende, 1993). The variation in composition of anurans in the rice fields and Reserva Lake during the study period was analysed using Principal Components Analysis (PCA) (Goodall, 1954), in PC-ORD Version 4.2 (McCune and Mefford, 2006). In the ordination analysis, the rice fields were separated according to the management practice (flooded and dry) in order to highlight possible differences in the temporal succession of the anuran composition. The ordination was performed using the abundance of flooded rice fields (n 5 3), dry rice fields (n 5 3) and Reserva Lake (n 5 3) over the study period. Only species occurring in more than two collections were included in the analysis. The difference between flooded rice fields (n 5 3), dry rice fields (n 5 3) and Reserva Lake (n 5 3) for the anuran species composition was verified by MRPP (Multi-Response Permutation Procedures) (PC-ORD 4.0, McCune and Mefford, 2006). The MRPP tests differences between two or more groups. For MRPP analyses, the chance-corrected within-group agreement (A) describes within-group homogeneity compared with the random expectation. When all samples are identical within groups, A 5 1, and when heterogeneity within groups equals that expected by random chance, A 5 0. If there was more heterogeneity within groups than expected by chance, Ao0. Indicator Species Analysis (Dufrene and Legendre, 1997) was used to determine the relative abundance and fidelity of a species to particular rice management practices (flooded and dry) and Reserva Lake over the study period. The significance of the discriminating power was determined by the Monte-Carlo test (5000 permutations).
RESULTS Twelve species distributed among five anuran families were collected during the study period in the rice fields (12 species) and in Reserva Lake (nine species). The families with highest representation in the surveys were Hylidae (five and four, respectively), followed by Leiuperidae (three species) and Leptodactylidae (two and one species, respectively). Two families were represented only by a single species: Bufonidae (Rhinella fernandezae was found in rice fields and Reserva Lake) and Cycloramphidae (Odontophrynus maisuma was found only in rice fields). In total, 2139 anuran individuals Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 39–46 (2010) DOI: 10.1002/aqc
42
I.F. MACHADO AND L. MALTCHIK
were observed in rice fields (798) and Reserva Lake (1341). Hylidae represented the majority of the individuals observed in rice fields (293) and in Reserva Lake (859), followed by Leptodactylidae (270 and 222, respectively), and Leiuperidae (201 and 231, respectively) (Table 1). Dendropsophus minutus was sampled in one collection only. One specimen of Chthonerpeton indistinctum (Reinhardt and Lu¨tken, 1862) (Amphibia: Gymnophiona) was also found in Reserva Lake. The total anuran richness ranged from two to eight species in rice fields, and from five to eight species in Reserva Lake during the study period. The mean anuran richness changed over time in rice fields and in Reserva Lake (F5,30 5 5.752; P 5 0.001), and it was higher in the growing seasons (1 and 2) than in the first fallow collection and after harvesting (Tukey, Po0.05). The mean anuran richness was similar between flooded and dry rice fields (F1,4 5 2.174, P 5 0.214), and there was no interaction between management practices and rice cultivation phases (F5,20 5 0.620, P 5 0.686), except in fallow 1, when the mean richness was higher in flooded than in dry rice fields (Figure 2(a)). The mean anuran richness was higher in Reserva Lake than in flooded and dry rice fields (F2,6 5 14.390, P 5 0.005), and also there was no interaction between systems (flooded and dry rice fields and Reserva Lake) and time (F10,30 5 1.349, P 5 0.251) (Figure 2(a)). The total anuran abundance ranged from 3 to 66 individuals in rice fields, and from 54 to 139 individuals in Reserva Lake over the study period. The mean abundance changed over time in rice fields and Reserva Lake (F5,30 5 26.199, Po0.001), and it was higher in the growing seasons (1 and 2) than in the other collections during the study period (Tukey, Po0.05). The lowest values for abundance were found in fallow phases (1 and 2) and after the harvesting phase (Tukey, Po0.05). The mean anuran abundance was similar between flooded and dry rice fields (F1,4 5 4.414, P 5 0.104). However, there was interaction between management practices and rice cultivation phases
Table 1. Cumulative number of individuals per anuran species in rice fields and Reserva Lake observed over the annual rice cultivation cycle (2005/2006) Species
Abundance Flooded rice fields
Bufonidae Rhinella fernandezae Cycloramphidae Odontophrynus maisuma Hylidae Dendropsophus minutus Dendropsophus sanborni Hypsiboas pulchellus Pseudis minuta Scinax squalirostris Leptodactylidae Leptodactylus gracilis Leptodactylus ocellatus Leiuperidae Physalaemus biligonigerus Pseudopaludicola falcipes Physalaemus gracilis Total Richness Total Abundance
Dry rice fields
Reserva Lake
14
15
29
4
1
0
0 27 31 174 6
3 16 3 33 0
0 163 189 306 201
0 136
14 120
0 222
17 57 11
8 105 3
15 179 37
10 477
11 321
9 1341
Copyright r 2009 John Wiley & Sons, Ltd.
(F5,20 5 3.429, P 5 0.021); the abundance was higher in flooded than in dry rice fields in fallow 1 and in growing season 1 (Figure 2(b)). The mean abundance was higher in Reserva Lake than in flooded and dry rice fields over the study period (F10,30 5 2.849, P 5 0.013) (Figure 2(b)). The first three axes generated by PCA explained 71.3% of the variation in anuran composition (41.03% first and 18.59% second axis) in flooded and dry rice fields and in Reserva Lake over the study period (Figure 3). The anuran composition in flooded rice fields was different from that in dry rice fields over the cultivating cycle (MRPP: A 5 0.1037; P 5 0.012), and it was different between the rice fields (flooded1dry) and Reserva Lake (MRPP: A 5 0.3401; Po0.001) (Figure 3). The anuran composition of Reserva Lake was different from the composition found in the flooded rice fields (MRPP: A 5 0.2762; P 5 0.001) and in dry rice fields (MRPP: A 5 0.3983; P 5 0.0006) (Figure 3). While Leptodactylus gracilis was more abundant in rice fields (flooded and dry), Leptodactylus ocellatus, Physalaemus biligonigerus, and Rhinella fernandezae were associated with flooded rice fields in the growing phase. The density of the other species was higher in Reserva Lake (Figure 3). The change in the anuran composition between flooded and dry rice fields was observed mainly in the tillage and rice growing phase 1 (Figure 3). The anuran composition after the harvesting phase (D6 and F6) was similar to the composition of the fallow phases in rice fields (flooded and dry–D1, D2 and D6, and F1, F2 and F6). Pseudopaludicola falcipes (IV 5 52.5), Pseudis minuta (IV 5 59.6), Dendropsophus sanborni (IV 5 79.1), Hypsiboas pulchellus (IV 5 84.8) and Scinax squalirostris (IV 5 97.1) were indicator species for Reserva Lake (Indicator Species Analysis, Po0.05).
DISCUSSION Twelve anuran species were found in rice fields, representing more than 13% of the richness from natural wetlands in southern Brazil, and 75% of the richness observed in the study region (Loebmann, 2005; Machado and Maltchik, 2007, respectively). However, the composition of the species observed in Reserva Lake was different from that in rice fields, mainly due to the high dominance of hylids and leptodactylids, which corresponded to about 50% of the total observed species. In this study, it was observed that some anuran species reproduced in both natural wetlands and rice fields. Vocalizations, tadpoles and metamorphosing individuals of D. sanborni, H. pulchellus, L. ocellatus, P. biligonigerus, P. falcipes, P. minuta, R. fernandezae and S. squalirostris were observed in both systems. No species of conservation concern were recorded in either habitat; however, there is only one listed species found in the Coastal Plain (Melanophryniscus dorsalis). The majority of the species in the study region use rice fields as complementary habitat, either as reproductive habitat or as movement corridors linking adjacent natural wetlands (Brode and Bury, 1984; Semlitsch and Bodie, 2003). Further studies are necessary to evaluate the real use of these systems by the anuran community. Anuran richness and abundance changed over the rice cultivating cycle, and the highest value was observed during growing phases (G1 and G2). The largest amphibian richness and abundance coincided with the summer (high temperatures) Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 39–46 (2010) DOI: 10.1002/aqc
MANAGEMENT PRACTICES IN RICE FIELDS AND AMPHIBIAN CONSERVATION
43
Figure 2. (a) Anuran mean richness (7SD) in the study rice fields (dry and flooded) and in Reserva Lake during the 2005/2006 cultivating cycle; and (b) anuran mean abundance (7SD) in the flooded and dry fields and in Reserva Lake during the 2005/2006 cultivating cycle.
and with the occurrence of surface water during the growing phases. The anuran assemblages are strongly influenced by air temperature and hydroperiod (Pechmann et al., 1989; Duellman and Trueb, 1994; Bertoluci and Rodrigues, 2002). Temperature influences several amphibian physiological and behavioural processes, such as water balance, calling, metamorphosis, development and immune response (Rome et al., 1992). The hydroperiod is one of the most important factors determining species richness, productivity and habitat suitability for pondbreeding amphibians (Babbitt and Tanner, 2000). Variations in water level may affect the abundance and diversity of species of amphibians in wetland systems (Pechmann et al., 1989). In the present study, the largest richness and abundance of amphibians was also associated with the observed reproductive period of species in southern Brazil (Achaval and Olmos, 1997; Kwet and Di Bernardo, 1999). In the study rice fields, the control of aquatic plants with herbicide was carried out during the tillage phase and at the beginning of the growing season. Glyphosate, one of the main herbicides used in rice fields, is a non-selective systemic herbicide used to kill weeds, especially sedges and grasses (Baird et al., 1971; Shibayama, 2001). Recent studies have shown that tadpoles are one of the vertebrate groups most Copyright r 2009 John Wiley & Sons, Ltd.
sensitive to the toxic effects of glyphosate herbicides (Govindarajulu, 2008). Glyphosate herbicides cause sublethal effects on anuran communities, including reduced growth and development rates, behavioural impairment, and genomic effects (Govindarajulu, 2008). However, the population-level consequences of these sub-lethal effects have not been tested under field conditions (Govindarajulu, 2008). Despite this, no sign was found of detrimental effects of herbicides in the rice fields. However, if rice fields are to be used as conservation tools, the use of herbicides and other chemicals must be carefully evaluated. The hydroperiod is an important determinant factor for anuran composition in wetland systems (Pechmann et al., 1989; Moreira et al., 2007). In the present study, some species (e.g. Hypsiboas pulchellus, Scinax squalirostris, Pseudopaludicola falcipes, and Pseudis minuta) were important to discriminate flooded, dry rice fields and Reserva Lake. The variation in anuran composition followed a similar pattern along the cultivating cycle (in both management practices — flooded and dry rice fields). Anuran composition after the harvesting phase was very similar to the composition found during the fallow phases. This indicated that species composition in these agroecosystems tended to return to the initial condition after Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 39–46 (2010) DOI: 10.1002/aqc
44
I.F. MACHADO AND L. MALTCHIK
Figure 3. Principal Component Analysis (PCA) ordination plot of rice fields (flooded and dry fields during the fallow phase) and Reserva Lake based on the anuran composition on each sampling occasion for the cultivating cycle 2005/2006. F 5 flooded rice fields, D 5 dry rice fields, R 5 Reserva Lake; 1 5 Fallow phase 1 (Jun/05); 2 5 Fallow phase 2 (Sep/05); 3 5 Tillage phase (Nov/05); 4 5 beginning of growing season — rice emergence (Jan/06); 5 5 end of growing season — rice tilling (Mar/06); 6 5 after harvesting (Jun/06).
the rice cultivating period, indicating a strong seasonality to anuran presence in rice fields in southern Brazil. The different management practices adopted after the harvesting period (presence or lack of surface water) did not influence the anuran richness and abundance; however, it influenced the composition. Studies that analyse the dynamics of aquatic organisms in rice fields and that compare different hydrologic management practices are scarce, and most of them focus on the zooplankton and bird community in temperate regions (Kurasawa, 1956; Rossi et al., 1974; Elphick et al., 2007; Manley, 2008). The results of this study show that even though management practices in rice fields produced similar anuran richness and abundance, species composition was different between the study areas. Lack of surface water in dry rice fields during most of the cultivating cycle favoured the development of terrestrial species, such as Bufonidae, Cycloramphidae, and Leptodactylidae. In rice fields that remained flooded, hylids were more abundant. Thus, the mosaic created by the variation of wetlands and dry lands resulting from rice culture is appropriate to preserve a high diversity of anurans. The difference in species composition between the adopted management practices is an interesting result in terms of biodiversity conservation. Rice producers could maintain part of their agricultural land flooded during the fallow phase. The existence of dry and flooded rice fields during the fallow phase may help to support auxiliary populations of anurans that will re-colonize natural adjacent wetlands, thereby enhancing biodiversity in these systems. These results should be taken into consideration in wetland conservation plans in southern Copyright r 2009 John Wiley & Sons, Ltd.
Brazil. Managing rice fields to maximize their utility as amphibian habitat could effectively increase the amount of wetland habitat available in southern Brazil by 30% and would represent a powerful conservation action. This study suggests that rice fields can help to conserve an important fraction of the amphibian richness in wetlands of southern Brazil, acting as refuges for biodiversity. However, the rice fields must not be viewed as surrogate systems for natural wetlands, given that the more complex natural systems play an important part in aquifer recharge, climatic stability and water storage. Furthermore, the anuran richness, abundance and composition were different between natural and artificial wetlands. Nevertheless the management practices proposed here could be an important strategy for biodiversity conservation in areas that are not established as Units of Conservation. Such a strategy would reconcile agricultural and economic needs with the conservation of biodiversity in southern Brazil, where more than 90% of wetland systems have already been lost and those remaining are at high risk owing to the expansion of rice production.
ACKNOWLEDGEMENTS This research was supported by funds from UNISINOS (02.00.023/00-0) and CNPq (52370695.2). Leonardo Maltchik holds a Brazilian Research Council CNPq Research Productivity grant. Aline Regina Gomes Moraes Lace helped in the field surveys. Dr Alexandre Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 39–46 (2010) DOI: 10.1002/aqc
MANAGEMENT PRACTICES IN RICE FIELDS AND AMPHIBIAN CONSERVATION
F. Souza (UNISINOS) and Dr Elvio S. F. Medeiros (UEPB) are thanked for collaboration in the revision and suggestions to this manuscript. We also thank two anonymous referees, and the landowners who allowed access to rice fields on their properties. We declare that the data collection complied with the Brazilian current laws.
REFERENCES Achaval F, Olmos A. 1997. Anfibios e Reptiles del Uruguay. Facultad de Ciencias Universad de la Republica Oriental del Uruguay: Montevideo, Uruguay. Azambuja IHV, Vernetti JFJ, Magalha˜es JAM. 2004. Aspectos socioeconoˆmicos da produc- a˜o do arroz. In Arroz irrigado no Sul do Brasil, Gomes AS, Magalha˜es JAM (eds). Embrapa Informac- a˜o Tecnolo´gica: Brası´ lia; 23–44. Babbitt KJ, Tanner GW. 2000. Use of temporary wetlands by anurans in a hydrologically modified landscape. Wetlands 20: 313–322. Baird D, Upchurch R, Homesly W, Franz J. 1971. Introduction of a new broad spectrum postemergence herbicide class with utility for herbaceous perennial weed control. In Proceedings of the 26th North Central Weed Control Conference, North Central Weed Science Society, Kansas City; 64–68. Bambaradeniya CNB, Amerasinghe FP. 2003. Biodiversity associated with the rice field agroecosystem in Asian countries: a brief review. International Water Management Institute 63: 1–29. Bertoluci J, Rodrigues MT. 2002. Seasonal patterns of breeding activity of Atlantic Rainforest anurans at Borace´ia, Southeastern Brazil. Amphibia-Reptilia 23: 161–167. Brasil. 2006. Third National Report to the Convention on Biological Diversity. Ministe´rio do Meio Ambiente: Brası´ lia. Brode JM, Bury RB. 1984. The importance of riparian systems to amphibians and reptiles. In California Riparian Systems. Ecology, Conservation, and Productive Management, Warner RE, Hendrix KM (eds). University of California Press: Berkeley; 30–36. Brouder SM, Hill JE. 1995. Winter flooding of ricelands provides waterfowl habitat. California Agriculture 49: 1–58. Burhanuddin MN. 1993. Use and management of riverine wetlands and rice fields in Peninsula Malaysia. In Towards Wise Use of Asian Wetlands, Isozaki H, Ando M, Natori Y (eds). Proceedings of the Asian Wetland Symposium, International Lake Environment Committee Foundation, Kusitsu City, Japan; 15–20. Cei JM. 1980. Amphibians of Argentina. Monitore Zoologico Italiano 2: 1–609. Czech HA, Parsons KC. 2002. Agricultural wetlands and waterbirds: a review. Waterbirds 25: 56–65. Davis TJ, Blasco D, Carbonell M. 1996. Manual de la Convencion de Ramsar. Una guia a la Convencion sobre los humedales de importancia internacional. Oficina de la Convencio´n de Ramsar: Gland. Dodd KC. 1992. Biological diversity of a temporary pond herpetofauna in north Florida sandhills. Biodiversity and Conservation 1: 125–142. Dodd KC, Cade BS. 1998. Movement patterns and the conservation of amphibians breeding in small, temporary wetlands. Conservation Biology 12: 331–339. Duellman WE, Trueb L. 1994. Biology of Amphibians. The Johns Hopkins University Press: Baltimore. Copyright r 2009 John Wiley & Sons, Ltd.
45
Dufrene M, Legendre P. 1997. Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecological Monographs 67: 345–366. Elphick CS, Oring LW. 1998. Winter management of Californian rice fields waterbird comment. Journal of Applied Ecology 35: 95–108. Elphick CS, Oring LW. 2003. Conservation implications of flooding rice fields on winter waterbird communities. Agriculture Ecosystems and Environment 94: 17–29. Elphick CS, Zuur AF, Ieno EN. 2007. Investigating the effects of rice farming on aquatic birds with mixed modelling. In Analysing Ecological Data, Zuur AF, Ieno EN, Smith GM (eds). Springer: New York; 417–434. FAO Stat. 2004. FAO Statistical Databases. Available online at http://apps.fao.org. Fernando CH, Furtado JI, Lim RP. 1979. Aquatic fauna of the world’s rice fields. Wallaceana Supplement Kuala Lumpur 2: 1–105. Fujioka M, Lane SJ. 1997. The impact of changing irrigation practices in rice fields on frog populations of the Kanto Plain, central Japan. Ecological Research 12: 101–108. Getzner M. 2002. Investigating public decisions about protecting wetlands. Journal of Environmental Management 64: 237–246. Gomes ADS, Magalha˜es AMD. 2004. Arroz irrigado no Sul do Brasil. Embrapa: Pelotas. Goodall DW. 1954. Objective methods for the classification of vegetation. III. An essay in the use of factor analysis. Australian Journal of Botany 2: 304–324. Govindarajulu PP. 2008. Literature review of impacts of glyphosate herbicide on amphibians: what risks can the silvicultural use of this herbicide pose for amphibians in B.C.? B.C. Ministry of Environment, Victoria, BC. Wildlife Report No. R-28. Guadagnin DL, Maltchik L. 2007. Habitat and landscape factors associated with Neotropical waterbird occurrence and richness in wetland fragments. Biodiversity and Conservation 16: 1231–1244. IRGA. 2007. Arroz irrigado: safra 2006/2007 – produc- a˜o municipal. Instituto Riograndense do Arroz. Sec- a˜o de Polı´ tica Setorial–DCI: Porto Alegre. Juliano BO. 1993. Rice in Human Nutrition. Food and Agriculture Organization (FAO) and International Rice Research Institute (IRRI): Manila, Philippines. Kurasawa H. 1956. The weekly succession in the standing crop of plankton and zoobenthos in the paddy field. Miscellaneous Reports of the Research Institute for Natural Resources. Tokyo. 4(41/42), 86–98 (in Japanese). Kwet A, Di-Bernardo M. 1999. Pro´-Mata-Anfı´bios. Amphibien. Amphibians. EDIPUCRS: Porto Alegre. Loebmann D. 2005. Guia Ilustrado: Os anfı´bios da regia˜o costeira do extremo sul do Brasil. USEB: Pelotas. Machado IF, Maltchik L. 2007. Check-list da diversidade de anuros no Rio Grande do Sul (Brasil) e proposta de classificac- a˜o para as formas larvais. Neotropical Biology and Conservation 2: 101–116. Maltchik L. 2003. Three new wetlands inventories in Brazil. Interciencia 28: 421–423. Maltchik L, Costa ES, Becker CG, Oliveira AE. 2003. Inventory of wetlands of Rio Grande do Sul (Brazil). Pesquisas: Botaˆnica 53: 89–100. Manley SW. 2008. Conservation in Ricelands of North America. The Rice Foundation. McCune B, Mefford MJ. 2006. PC-ORD. Multivariate Analysis of Ecological Data. Version 5.10 MjM Software, Gleneden Beach, Oregon. Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 39–46 (2010) DOI: 10.1002/aqc
46
I.F. MACHADO AND L. MALTCHIK
Millennium Ecosystem Assessment. 2005. Ecosystems and Human Well-Being: Wetlands and Water Synthesis. World Resources Institute: Washington, DC. Miller RR, Williams JD, Williams JE. 1989. Extinctions of North American fishes during the past century. Fisheries 14: 22–38. Moler PE, Franz R. 1987. Wildlife values of small, isolated wetlands in the Southeastern coastal plain. In Proceedings of the Third Nongame and Endangered Wildlife Symposium, Odom RR, Riddleberger KA, Ozier JC (eds). Georgia Department of Natural Resources; 234–241. Moreira LFB, Machado IF, Lace ARGM, Maltchik L. 2007. Calling period and reproductive modes in an anuran community of a temporary pond in Southern Brazil. South American Journal of Herpetology 2: 129–135. Neiff JJ. 2001. Diversity in some tropical wetland systems of South America. In Biodiversity in Wetlands: Assessment, Function and Conservation, Gopal B, Junk WJ, Davis JA (eds). Backhuys Publishers: Leiden. Pechmann JHK, Scott DE, Gibbons JW, Semlitsch RD. 1989. Influence of wetland hydroperiod on diversity and abundance of metamorphosing juvenile amphibians. Wetlands Ecology and Management 1: 3–11. Rambo B. 2000. A fisionomia do Rio Grande do Sul: ensaio de monografia natural. Unisinos: Sa˜o Leopoldo. Rodrigues ASL, Andelman SJ, Bakarr MI, Boitani L, Brooks TM, Cowling RM, Fishpool LDC, Fonseca GAB, Gaston KJ, Hoffmann M et al. 2004. Effectiveness of the global protected area network in representing species diversity. Nature 428: 640–643. Rolon AS, Maltchik L. 2006. Environmental factors as predictors of aquatic macrophyte richness and composition in wetlands of southern Brazil. Hydrobiologia 556: 221–231. Rolon AS, Lacerda T, Maltchik L, Guadagnin DL. 2008. The influence of area, habitat and water chemistry on richness and composition of macrophyte assemblages in southern Brazil wetlands. Journal of Vegetation Science 19: 221–228. Rome LC, Stevens ED, John-Adler HB. 1992. The influence of temperature and thermal acclimation on physiological
Copyright r 2009 John Wiley & Sons, Ltd.
function. In Environmental Physiology of the Amphibians, Feder ME, Burggren WW (eds). University of Chicago Press: Chicago; 183–205. Rosset SD. 2008. New species of Odontophrynus Reinhardt and Lu¨tken 1862 (Anura: Neobatrachia) from Brazil and Uruguay. Journal of Herpetology 42: 134–144. Rossi O, Moroni A, Baroni P, Caravello U. 1974. Annual evolution of the zooplankton diversity in twelve Italian ricefields. Bollettino di Zoologia 41: 157–181. SBH. 2009. Brazilian amphibians — List of species. Accessible at http://www.sbherpetologia.org.br. Sociedade Brasileira de Herpetologia. Captured on 22/apr/2009. Semlitsch RD. 1998. Biological determination of terrestrial buffer zones for pond-breeding salamanders. Conservation Biology 12: 1113–1119. Semlitsch RD, Bodie JR. 2003. Biological criteria for buffer zones around wetlands and riparian habitats for amphibians and reptiles. Conservation Biology 17: 1219–1228. Shibayama H. 2001. Weeds and weed control management in rice production in Japan. Weed Biology and Management 1: 53–60. Silvano DL, Segalla MV. 2005. Conservation of Brazilian amphibians. Conservation Biology 19: 653–658. SPSS. 2002. Statistical Package for Social Sciences. Chicago. Stenert C, Maltchik L. 2007. Influence of area, altitude and hydroperiod on macroinvertebrate communities in southern Brazil wetlands. Marine and Freshwater Research 58: 993–1001. Stenert C, Bacca RC, Mostardeiro CC, Maltchik L. 2008. Environmental predictors of macroinvertebrate communities in coastal wetlands of southern Brazil. Marine and Freshwater Research 59: 540–548. Tagliani PRA. 1995. Estrate´gia de Planificac- a˜o Ambiental para o Sistema Ecolo´gico da Restinga da Lagoa dos Patos — Planı´ cie Costeira do Rio Grande do Sul. PhD thesis, Universidade Federal de Sa˜o Carlos, Sa˜o Carlos, Brazil. von Ende CN. 1993. Repeated-measures analysis: growth and other time dependent measures. In The Design and Analysis of Ecological Experiments, Scheiner S, Gurevitch I (eds). Chapman and Hall; 113–137.
Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 39–46 (2010) DOI: 10.1002/aqc
