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Are aquatic insect species sensitive to banana plant cultivation?
Ecological Indicators 25 (2013) 156–161
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Are aquatic insect species sensitive to banana plant cultivation? Juliano José Corbi a,∗ , Priscila Kleine b , Susana Trivinho-Strixino b a b
Departamento de Hidráulica e Saneamento, Escola de Engenharia de São Carlos (EESC), Universidade de São Paulo – USP, C.P. 359, CEP 13566-590, São Carlos, SP, Brazil Departamento de Hidrobiologia, Universidade Federal de São Carlos, UFSCar. Cx. Postal 676, CEP 13565-905, São Carlos, SP, Brazil
a r t i c l e
i n f o
Article history: Received 12 June 2012 Received in revised form 17 August 2012 Accepted 23 September 2012 Keywords: EPTC fauna Preserved streams Indicator species Banana streams
a b s t r a c t Ephemeroptera, Plecoptera, Trichoptera and Coleoptera (EPTC) insect fauna were collected in ten streams located in the southeastern state of São Paulo (five located in areas with banana cultivation and five located in preserved areas). Specimens were collected during October and November 2005, using a Surber sampler and network D (0.25 mm mesh size) in areas of rapids and backwaters. The organisms collected were identified to genus level, except for some small or damaged specimens that remained at the family level. In total, 1812 individuals of EPTC were identified, in which 1105 organisms were from streams in areas of banana cultivation and 706 from streams in preserved areas. Heterelmis (Elmidae) was dominant in both sets of streams. In preserved streams, Hexacylloepus (Elmidae), Tupiperla and Paragrypopteryx (Gripopterygidae) and Nectopsyche (Leptoceridae) also had high participation. Leptonema (Hydropsychidae) and Xenelmis (Elmidae) were dominant in streams located in areas of banana cultivation. The analyses of indicator species point out to five taxa on preserved streams and two taxa in the banana streams. The forested streams had higher richness and diversity of EPTC than banana plantation streams. Correspondence analysis point for two groups, one gathered in the streams near the banana plantation and the other in the preserved streams. The similarity test (ANOSIM) pointed to significant differences (P < 0.05) between these groups. This agricultural activity seems to influence the EPTC community structure in low order streams in the Atlantic Forest region. The identification of groups at the EPTC genus level was important to point out the differences between the fauna of streams impacted by banana cultivation and to establish indicator species. © 2012 Elsevier Ltd. All rights reserved.
1. Introduction Aquatic ecosystems have been impacted by innumerable anthropic actions, such as agricultural activities, hydrologic alterations and pollution, causing modifications in these systems (Allan et al., 1997) and changes in the faunistic structure (Pringle et al., 2000). Contaminations resulting from urban runoff, for example, exert a deleterious impact on freshwater macroinvertebrates particularly the loss of sensitive orders such as Ephemeroptera (mayflies), Plecoptera (stoneflies) and Trichoptera (caddisflies) (Karouna-Renier and Sparling, 2001; Corbi and Trivinho-Strixino, 2008). However, the assessment and quantification of the effects caused by anthropic impacts are difficult to evaluate because they can be confused with local, regional or temporal variations. The species richness of stream invertebrates is also strongly influenced by anthropogenic disturbances, which may lead to losses of taxa and cause spatial discontinuities in predictable gradients. Resh and Jackson (1993) observed that species richness is sensitive to the impact of human activities on stream
∗ Corresponding author. E-mail addresses: [email protected], [email protected] (J.J. Corbi). 1470-160X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecolind.2012.09.020
environments, mainly affecting that of aquatic insects of the orders Ephemeroptera, Plecoptera and Trichoptera (EPT), which are often good indicators of environmental conditions and stream characteristics (Crisci-Bispo et al., 2007). Hamid and Rawi (2011) showed that distribution of the EPT genera in the rivers of the Gunung Jerai catchment, a northern state in Peninsular Malaysia, was influenced by the availability of surface area on rocky substrates and the amount of light penetration in the water. A study conducted by Wallace et al. (1996), in southern Appalachian headwater streams, indicates that the EPT index was by far the easiest to use and easy to apply as biological indicators. The researchers strongly sustain the addition of the EPT indices in streams as indicators of both degradation and recovery of stream ecosystem processes from chemically induced disturbance. In the same way, the study conducted by Compin and Céréghino (2003) pointed to the fact that EPT species richness was significantly different in the whole-drainage-basin of Adour–Garonne stream system (South-Western-France). Wallace et al. (1996) have also noticed that the Ephemeroptera, Plecoptera and Trichoptera richness was stable at reference sites, and actually responded to variations of water quality. It is a good biological indicator of river quality, and it is also easy to measure since it is based on the only presence of species belonging to well-known groups of insects currently identified by specialists (Compin and Céréghino, 2003).
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As the aquatic insects like EPT may integrate effects of perturbations, numerous studies have been proposed to use stream insect communities to validate the effects of different land uses (Brabec et al., 2004), mining activities (Courtney and Clements, 2002) and agricultural activities, such as sugar cane cultivation and pasture (Bunn et al., 1997; Corbi and Trivinho-Strixino, 2008; Corbi et al., 2008, 2010) and banana cultivation (Kleine et al., 2012). However, studies on the possible impacts of the banana plant cultivation in aquatic insects are rare. In the banana culture, the maintenance of the vegetal covering provides shade on the stream of the adjacent areas and makes this culture different from other agriculture activities (Embrapa Mandioca et al., 2007). Moreover, small amounts of pesticides are used when compared to other agricultural activities. For example, in banana cultivation, 0.31 kg/ha/year of pesticides are used, while in sugarcane culture, 3.4 kg/ha/year is used and in apples, 49 kg/ha/year (Neves et al., 2002). Little is known about the consequences of the inadequate handling and of possible impacts of this culture, although this culture is found in extensive areas in São Paulo state, covering 545000 ha, mainly in Atlantic Forest (on the Brazilian coast), that is considered one of the most impacted ecosystems in the world (Bibby et al., 1992) and therefore considered as one world-wide hotspot (Myers et al., 2000). The present study focused on Ephemeroptera, Plecoptera, Trichoptera, and Coleoptera (EPTC), aquatic insects commonly identified in freshwater studies. Following Compin and Céréghino (2003), we added Coleoptera to the standard EPT index. Coleoptera are considerable major components of stream invertebrate assemblages and contain sensitive taxa particularly in the family Elmidae. Cayrou et al. (2000) have also recently showed the pertinence of EPTC species relations for stream classifications. We analyze ten streams (five located in areas with banana cultivation and five located in preserved areas). We also applied a simple method to find
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EPTC indicator species and species assemblages that characterize groups of sites (preserved or disturbed). 2. Materials and methods The study was conducted in the Vale do Ribeira, São Paulo state, Brazil, in the municipalities of Cananéia, Jacupiranga and Cajati, where banana cultivation is very intense (Fig. 1). The EPTC fauna were collected in 10 streams, during October and November of 2005. The studied streams are located between the coordinates 24◦ 50 (S) and 24◦ 59 (S) and 48◦ 00 (W) and 48◦ 59 (W). Aquatic macroinvertebrates of each stream were collected using a D-frame aquatic net (250 m) and a Surber sampler (250 m) including riffle and pool areas, for 5 min, as recommended by Fontoura (1985). In each stream, 9 samples were collected. Samples were taken to the laboratory, washed in a sieve of 250 m mesh, selected on an illuminated tray and fixed with 70% alcohol. The taxonomic identification was achieved at the genus level for most of the specimens, based on the available published data (Domínguez et al., 2006; Passos et al., 2007; Fernández and Domínguez, 2001; Lecci and Froehlich, 2007). In order to aid the evaluation of the integrity of the 10 streams, physical and chemical variables of the water were measured. Physical and chemical variables such as pH, temperature, dissolved oxygen and electric conductivity were measured in situ, by using a Water Quality Checker device (Horiba) (Table 1). 2.1. Data analysis With the aim of analyzing the integrity of each stream, the EPTC community characteristics were determined by % participation in the community, Shannon and Margalef diversities, and the dominance index of each taxon in the stream (Kownacki, 1971). For
Fig. 1. Map of São Paulo state and Satellite Image indicating the sampling sites in the region of Ribeira Valley and South Coast of São Paulo state, Brazil. Source: Atlas Biota and Google Earth.
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Table 1 General characteristics and location of the streams. Municipalities
a
Streams
Land use
Coordinates ◦
Width (m) ◦
Depth (cm)
Electric conductivity (S cm−1 )
Temp. (◦ C)
DO (mg L−1 )
Cajati
B1 B2
Banana cultivation Banana cultivation
S24 51 W48 05 S24◦ 50 W48◦ 14
1.50 1.27
7.0 4.0
b
na 1.50
22.7 21.2
7.80 10.30
Jacupiranga
B3 B4 B5
Banana cultivation Banana cultivation Banana cultivation
S24◦ 50 W48◦ 14 S24◦ 51 W48◦ 05 S24◦ 51 W48◦ 6
0.95 0.52 0.78
8.3 5.0 5.0
0.50 0.05 1.13
21.7 26.2 21.2
7.87 8.50 8.45
Cananéia
M1 M2 M3 M4 M5
Preserved Preserved Preserved Preserved Preserved
S24◦ 59 S25◦ 00 S24◦ 57 S24◦ 57 S24◦ 58
1.5 2.16 1.93 1.47 2.71
15.0 14.2 15.1 13.4 22.1
b
19.4 19.2 19.0 19.5 20.3
8.5 9.56 9.27 9.03 8.20
na 0.03 0.21 0.21 0.24
B = banana streams; M = preserved streams. na = not analyzed.
the data set (total EPTC of the 10 streams), a multivariate analysis of correspondence was applied to calculate the similarity between streams. The EPTC groups, which showed a close correlation, were identified and grouped to a further similarity test (ANOSIM). This test was used to detect significant differences between the two groups. For this analysis, 5% as p-level was considered. ANOSIM was calculated using Simpson as distance measure. The correspondence analysis and the ANOSIM were calculated by using the PAST Program (Version 1.68) (Hammer et al., 2001). We also applied a simple method to find indicator species characterizing groups of sites (preserved or disturbed). This analysis called indicator species analysis (ISA) (Dufrêne and Legendre, 1997), combines species relative abundance with its relative frequency of occurrence in the various groups of sites. This index is maximum when all individuals of a species are found in a single group of sites and when the species occurs in all sites of that group; it is a symmetric indicator. According to this technique, there are groups, in the data set, which can be indicated by some taxa. This analysis was made using the PC-ORD 4 (Mccune and Mefford, 1999) program and was validated by the Monte Carlo test, with 5000 permutations.
3. Results In total, 1812 individuals of EPTC were identified, in which 1105 organisms were in streams in areas of banana cultivation and 706 in preserved streams (Table 2). Heterelmis (Elmidae) was dominant in both sets of streams. Besides this, in preserved streams, Hexacylloepus (Elmidae), Tupiperla and Paragrypopteryx (Gripopterygidae) and Nectopsyche (Leptoceridae) also exhibited a notable presence. Leptonema (Hydropsychidae) and Xenelmis (Elmidae) were dominant in streams located in areas of banana cultivation (Table 2). The preserved streams had higher richness and diversity of EPTC than banana plantation streams. The main community characteristics are presented in Table 3. The correspondence analysis applied to the EPTC fauna delimited two groups: one grouping the assemblages in streams located in preserved areas (M1, M2, M3, M4 and M5) and the other one in streams in areas adjacent to banana plant cultivation (B1, B2, B3, B4 and B5) (Fig. 2). The test of similarity (ANOSIM) applied to the two groups, pointed to significant differences (p = 0.0083) between the situations. Dissolved oxygen (O2 ) also presented high concentrations in all streams with banana culture and in preserved areas. The values varied from 7.80 mg L−1 (B1 stream) to 10.30 mg L−1 (B2 stream), both located in areas with banana cultivation. Values of electric conductivity were slightly higher in areas with banana cultivation than preserved areas. The high value was detected for the B1 stream (0.03 S cm−1 ) and low value in M1 stream (1.50 S cm−1 ). The
1,6 1,2 0,8 0,4
Axis 2
a b
W48◦ 2 W48◦ 04 W48◦ 59 W48◦ 00 W48◦ 00
M4 M5 M2 M3 M1
B4
0
B5
B3
-0,4 -0,8 -1,2 -1,6 -2
B1 B2
-0,9 -0,6 -0,3
0
0,3
0,6
0,9
1,2
1,5
1,8
Axis 1 Fig. 2. Correspondence analysis applied for the EPTC species of the 10 streams. Legends as Table 1.
values of these components, as well as of the other measurements of physical and chemical characteristics, are presented in Table 1. The analyses of indicator species point to five species in preserved streams (Paragrypopteryx sp., Anacroneuria sp., Phylloicus sp., Triplectides sp. and Helicopsyche sp.) and two species in banana streams (Americabaetis sp. and Leptonema sp.) (Table 4). 4. Discussion Aquatic insects such as those in the EPTC orders known to be pollution-sensitive have been considered pertinent to use for stream classifications (Cayrou et al., 2000; Compin and Céréghino, 2003). According to these authors, EPTC is a good biological indicator of river quality, and it is also easy to measure since it is based on the only presence of species belonging to well-known groups of insects currently identified by specialists. The presence or the absence of many EPTC species whose ecology is well known (Vinc¸on and Thomas, 1987; Compin and Céréghino, 2003) could provide diagnostic clues when interpreting the score provided by the assessment method. In accordance with the researchers, in the field, only a qualitative sampling is required, thus the counting of sorted individuals is not necessary. By contrast, to verify the indicative value of taxa, quantitative samples are necessary. The five streams analyzed in banana areas had different distributions of EPTC species richness when compared to forested sites and the results also pointed to 7 species that would be used as indicator species from studied streams. So, our results justified the use of EPTC species indices for monitoring streams located in areas with
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Table 2 EPTC taxa collected in preserved and banana streams. Legends as Table 1. Taxa/streams
B1
B2
B3
B4
B5
M1
M2
M3
M4
M5
Chrysomelidae sp. Curculionidae Dryopidae sp. Pelonomus sp. Austrolimnius sp. Cylloepus sp. Heterelmis sp. Hexacylloepus sp. Macrelmis sp. Xenelmis sp. Phanocerus sp. Promoresia sp. Hydraena sp. Berosus sp. Paracymus sp. Lutrochus sp. Ectopria sp. Psephenus sp. Scirtidae sp.1 Scirtidae sp.2 Scirtidae sp.3 Staphylinidae sp. Grypopteryx sp. Tupiperla sp. Paragrypopteryx sp. Anacroneuria sp. Kempnyia sp. Ephemeroptera sp. Caenis sp. Americabaetis sp. Baetodes sp. Paracloeodes sp. Cryptonympha sp. Campylocia sp. Traverhyphes sp. Askola sp. Farrodes sp. Hylister sp. Leptohyphes sp. Miroculis sp. Thraulodes sp. Atopsyche sp. Phylloicus sp. Austrotinodes sp. Hydropsychidae sp. Blepharopus sp. Leptonema sp. Leptonema aff. sp. Macronema sp. Metrichia sp. Ochrotrichia sp. Oxyethira sp. Protoptila sp. Atanatolica sp. Nectopsyche sp. Triplectides sp. Barypenthus sp. Marilia sp. Chimarra sp. Cernotina sp. Polyplectropus sp. Helicopsyche sp. Xiphocentron sp.
– – 31 – 24 – 213 2 – 149 – – – 1 13 – 2 2 – – – 4 – – – – – – – 2 – – – – – – – – – – – – – – – – 41 – – 45 – – – 1 1 – – – 1 – – – 1
– – 1 – 2 – 17 1 – 91 – – – – 1 – 1 – – – 1 – 1 – – – – – – 2 2 – – – – – – – – – – 1 – – – – 2 – – 6 – – – – – – – – 1 – – – –
– 1 2 1 – – 17 26 – – – – 1 – 7 – – – – – – – – – – – – – – 4 – – – – – – – – – – – – – – – – 13 – – 2 1 – – – – – – – – – – – –
1 3 – – – 1 3 3 – – – – – 34 – – – – – – – – – – – – – – 41 40 – 2 – – 63 – 3 – – 4 – – – – – 3 64 – – 5 1 4 – – – – – – – – – – –
– – – – – 1 20 1 – – – – 1 – – – – – 1 – – – – 1 – – – – – 3 3 – – – 31 – – – – 1 – 1 – – – – 21 2 – – – – 2 – – – – – – – – – –
– – 2 – – – 19 11 2 – – – – – – – 1 – – – – – – 14 2 – – – – – – – – – – – 2 – – 7 – – 2 – – – 1 – – – – – – 1 – 1 – – 1 – – 1 –
– – 5 – 1 1 21 11 11 8 3 1 – 1 3 2 – – 2 1 – – – – 1 21 13 – – 1 – – 1 3 2 – – 1 – – 4 – 5 – 1 2 4 – – – – – – – 54 5 7 1 – – – 5 –
2 – – – – – 24 13 – – – – – – – – – – 1 – – – – – 3 7 – 13 – – – – – 4 – 9 3 – – 16 – 1 – – – 2 11 1 3 2 1 – – 1 4 2 – 1 1 8 2 13 –
– – – – – – 14 8 – – – – – – – – – – 4 3 – – – 30 21 3 2 – 1 2 – – 3 – – 6 6 3 – 26 – 1 1 1 – 10 4 – 7 2 – – – 2 8 2 – – – – – 2 –
1 – – – – – 17 14 – – – – 1 6 – – – 2 – 2 1 – – 23 18 2 2 – – – – – – – – 3 – – 3 – – – 1 – 1 8 – 1 – – 1 – – – – 3 2 – – – – 3 –
different land uses. In the same way, the low EPTC taxonomic resolution used in the present study clearly gave important information about the indicator taxa in the streams, specially for Plecoptera (Paragrypopteryx sp. and Anacroneuria sp.) and Trichoptera (Phylloicus sp., Triplectides sp. and Helicopsyche sp.) in the preserved streams, and Trichoptera Leptonema sp. and Ephemeroptera Americabaetis sp. in the disturbed streams. Although Coleoptera have been, in some cases, considerably good indicators of disturbed environments such as, for example, urban runoff, chemical pollution
and regulated flow (Compin and Céréghino, 2003), in the present study, this group does not present indicative value. Our results also show the importance of riparian vegetation, which provided a higher EPTC taxa richness in the forested streams (M1–M5) when compared to the areas with banana cultivation (B1–B5). Some factors like pollution, riparian vegetation and stream order, could have influenced the species richness of the studied streams, as observed by Diniz-Filho et al. (1998) in the central region of Brazil (Goiás state) and by Corbi and Trivinho-Strixino
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Table 3 Main community characteristics for the EPTC fauna of the 10 streams. Legends as Table 1.
EPTC family richness %Ephemeroptera %Plecoptera %Trichoptera %Coleoptera %EPTC Individuals Dominance D Shannon H Margalef Equitability J
B1
B2
19 0.7 0 7.57 38.1 46.07 534 0.26 1.72 2.87 0.59
16 0.97 0.24 2.43 28.0 31.63 130 0.51 1.24 3.08 0.45
B3 14 1.63 0 6.91 23,0 31.56 77 0.19 1.99 2.99 0.75
B4
B5
M1
M2
M3
M4
M5
21 21.21 0 7.04 7.7 46.77 275 0.16 2.15 3.56 0.71
15 26.26 0.56 15.08 13.9 51.45 89 0.23 1.82 3.12 0.67
16 7.26 12.90 5.65 28.5 54.47 67 0.16 2.21 3.57 0.80
35 3.66 10.98 25.61 22.5 62.46 204 0.11 2.82 6.58 0.79
28 16.73 3.72 19.70 15.4 56.92 148 0.08 2.85 5.40 0.86
31 12.24 14.58 10.42 7.6 44.91 172 0.09 2.87 5.83 0.84
24 2.88 18.52 8.23 18.6 47.93 116 0.11 2.57 4.84 0.81
Table 4 Indicator species in preserved and banana streams. IV (%) species indicator values; p value obtained by 5000 permutations (Monte Carlo Test). Taxa
Stream
IV (%)
p
Paragrypopteryx sp. Anacroneuria sp. Americabaetis sp. Phylloicus sp. Leptonema sp. Triplectides sp. Helicopsyche sp.
Preserved Preserved Banana Preserved Banana Preserved Preserved
100.0 80.0 94.4 80.0 87.6 100.0 100.0
0.0080 0.0410 0.0220 0.0460 0.0470 0.0080 0.0080
(2008) in streams located in areas with sugarcane cultivation and pastures, without riparian vegetation (Cerrado areas in the state of São Paulo). The deforestation of riparian vegetation also appeared to be reflected in the high values of temperature observed in the water of the impacted streams (B1–B5). The higher temperature observed in the deforested streams compared to the preserved ones appeared to also reflect in the values of dissolved oxygen in the water measured. The concentrations of cations (Mg, Mn, Na, K) are the components that influence the values of electric conductivity of the streams. Results obtained for the values of electric conductivity, also appeared to be a reflection of agricultural activities. In the deforested streams located in agricultural areas, the input of fertilizers (N, P, K) containing metals as micronutrients, probably influenced the high values of this variable in the water as observed for streams located in areas with banana plant cultivation.
5. Conclusions These results show the potential use of EPTC invertebrate taxa for detect agriculture impacts, especially banana plant cultivation. In the present study, the application of species indicator method, as proposed by Dufrene and Legendre, gives precise and accurate information on EPTC species and discriminate seven indicator species. The species identification obtained here could also become useful for agriculture impact assessment. Furthermore, our results demonstrate the importance of the preservation of riparian vegetation for the EPTC community’s distribution, which appeared to be the most important factor influencing the composition of these aquatic fauna and are also responsible for absorption of toxic products which come from the neighboring cultivated areas.
Acknowledgements The authors gratefully acknowledge the fruitful suggestions of Professor Pedro P. Corbi and Dra. Vanessa Colombo Corbi. We thank the National Council for Scientific and Technological Development (CNPq), for a research fellowship.
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Are aquatic insect species sensitive to banana plant cultivation? Juliano José Corbi a,∗ , Priscila Kleine b , Susana Trivinho-Strixino b a b
Departamento de Hidráulica e Saneamento, Escola de Engenharia de São Carlos (EESC), Universidade de São Paulo – USP, C.P. 359, CEP 13566-590, São Carlos, SP, Brazil Departamento de Hidrobiologia, Universidade Federal de São Carlos, UFSCar. Cx. Postal 676, CEP 13565-905, São Carlos, SP, Brazil
a r t i c l e
i n f o
Article history: Received 12 June 2012 Received in revised form 17 August 2012 Accepted 23 September 2012 Keywords: EPTC fauna Preserved streams Indicator species Banana streams
a b s t r a c t Ephemeroptera, Plecoptera, Trichoptera and Coleoptera (EPTC) insect fauna were collected in ten streams located in the southeastern state of São Paulo (five located in areas with banana cultivation and five located in preserved areas). Specimens were collected during October and November 2005, using a Surber sampler and network D (0.25 mm mesh size) in areas of rapids and backwaters. The organisms collected were identified to genus level, except for some small or damaged specimens that remained at the family level. In total, 1812 individuals of EPTC were identified, in which 1105 organisms were from streams in areas of banana cultivation and 706 from streams in preserved areas. Heterelmis (Elmidae) was dominant in both sets of streams. In preserved streams, Hexacylloepus (Elmidae), Tupiperla and Paragrypopteryx (Gripopterygidae) and Nectopsyche (Leptoceridae) also had high participation. Leptonema (Hydropsychidae) and Xenelmis (Elmidae) were dominant in streams located in areas of banana cultivation. The analyses of indicator species point out to five taxa on preserved streams and two taxa in the banana streams. The forested streams had higher richness and diversity of EPTC than banana plantation streams. Correspondence analysis point for two groups, one gathered in the streams near the banana plantation and the other in the preserved streams. The similarity test (ANOSIM) pointed to significant differences (P < 0.05) between these groups. This agricultural activity seems to influence the EPTC community structure in low order streams in the Atlantic Forest region. The identification of groups at the EPTC genus level was important to point out the differences between the fauna of streams impacted by banana cultivation and to establish indicator species. © 2012 Elsevier Ltd. All rights reserved.
1. Introduction Aquatic ecosystems have been impacted by innumerable anthropic actions, such as agricultural activities, hydrologic alterations and pollution, causing modifications in these systems (Allan et al., 1997) and changes in the faunistic structure (Pringle et al., 2000). Contaminations resulting from urban runoff, for example, exert a deleterious impact on freshwater macroinvertebrates particularly the loss of sensitive orders such as Ephemeroptera (mayflies), Plecoptera (stoneflies) and Trichoptera (caddisflies) (Karouna-Renier and Sparling, 2001; Corbi and Trivinho-Strixino, 2008). However, the assessment and quantification of the effects caused by anthropic impacts are difficult to evaluate because they can be confused with local, regional or temporal variations. The species richness of stream invertebrates is also strongly influenced by anthropogenic disturbances, which may lead to losses of taxa and cause spatial discontinuities in predictable gradients. Resh and Jackson (1993) observed that species richness is sensitive to the impact of human activities on stream
∗ Corresponding author. E-mail addresses: [email protected], [email protected] (J.J. Corbi). 1470-160X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ecolind.2012.09.020
environments, mainly affecting that of aquatic insects of the orders Ephemeroptera, Plecoptera and Trichoptera (EPT), which are often good indicators of environmental conditions and stream characteristics (Crisci-Bispo et al., 2007). Hamid and Rawi (2011) showed that distribution of the EPT genera in the rivers of the Gunung Jerai catchment, a northern state in Peninsular Malaysia, was influenced by the availability of surface area on rocky substrates and the amount of light penetration in the water. A study conducted by Wallace et al. (1996), in southern Appalachian headwater streams, indicates that the EPT index was by far the easiest to use and easy to apply as biological indicators. The researchers strongly sustain the addition of the EPT indices in streams as indicators of both degradation and recovery of stream ecosystem processes from chemically induced disturbance. In the same way, the study conducted by Compin and Céréghino (2003) pointed to the fact that EPT species richness was significantly different in the whole-drainage-basin of Adour–Garonne stream system (South-Western-France). Wallace et al. (1996) have also noticed that the Ephemeroptera, Plecoptera and Trichoptera richness was stable at reference sites, and actually responded to variations of water quality. It is a good biological indicator of river quality, and it is also easy to measure since it is based on the only presence of species belonging to well-known groups of insects currently identified by specialists (Compin and Céréghino, 2003).
J.J. Corbi et al. / Ecological Indicators 25 (2013) 156–161
As the aquatic insects like EPT may integrate effects of perturbations, numerous studies have been proposed to use stream insect communities to validate the effects of different land uses (Brabec et al., 2004), mining activities (Courtney and Clements, 2002) and agricultural activities, such as sugar cane cultivation and pasture (Bunn et al., 1997; Corbi and Trivinho-Strixino, 2008; Corbi et al., 2008, 2010) and banana cultivation (Kleine et al., 2012). However, studies on the possible impacts of the banana plant cultivation in aquatic insects are rare. In the banana culture, the maintenance of the vegetal covering provides shade on the stream of the adjacent areas and makes this culture different from other agriculture activities (Embrapa Mandioca et al., 2007). Moreover, small amounts of pesticides are used when compared to other agricultural activities. For example, in banana cultivation, 0.31 kg/ha/year of pesticides are used, while in sugarcane culture, 3.4 kg/ha/year is used and in apples, 49 kg/ha/year (Neves et al., 2002). Little is known about the consequences of the inadequate handling and of possible impacts of this culture, although this culture is found in extensive areas in São Paulo state, covering 545000 ha, mainly in Atlantic Forest (on the Brazilian coast), that is considered one of the most impacted ecosystems in the world (Bibby et al., 1992) and therefore considered as one world-wide hotspot (Myers et al., 2000). The present study focused on Ephemeroptera, Plecoptera, Trichoptera, and Coleoptera (EPTC), aquatic insects commonly identified in freshwater studies. Following Compin and Céréghino (2003), we added Coleoptera to the standard EPT index. Coleoptera are considerable major components of stream invertebrate assemblages and contain sensitive taxa particularly in the family Elmidae. Cayrou et al. (2000) have also recently showed the pertinence of EPTC species relations for stream classifications. We analyze ten streams (five located in areas with banana cultivation and five located in preserved areas). We also applied a simple method to find
157
EPTC indicator species and species assemblages that characterize groups of sites (preserved or disturbed). 2. Materials and methods The study was conducted in the Vale do Ribeira, São Paulo state, Brazil, in the municipalities of Cananéia, Jacupiranga and Cajati, where banana cultivation is very intense (Fig. 1). The EPTC fauna were collected in 10 streams, during October and November of 2005. The studied streams are located between the coordinates 24◦ 50 (S) and 24◦ 59 (S) and 48◦ 00 (W) and 48◦ 59 (W). Aquatic macroinvertebrates of each stream were collected using a D-frame aquatic net (250 m) and a Surber sampler (250 m) including riffle and pool areas, for 5 min, as recommended by Fontoura (1985). In each stream, 9 samples were collected. Samples were taken to the laboratory, washed in a sieve of 250 m mesh, selected on an illuminated tray and fixed with 70% alcohol. The taxonomic identification was achieved at the genus level for most of the specimens, based on the available published data (Domínguez et al., 2006; Passos et al., 2007; Fernández and Domínguez, 2001; Lecci and Froehlich, 2007). In order to aid the evaluation of the integrity of the 10 streams, physical and chemical variables of the water were measured. Physical and chemical variables such as pH, temperature, dissolved oxygen and electric conductivity were measured in situ, by using a Water Quality Checker device (Horiba) (Table 1). 2.1. Data analysis With the aim of analyzing the integrity of each stream, the EPTC community characteristics were determined by % participation in the community, Shannon and Margalef diversities, and the dominance index of each taxon in the stream (Kownacki, 1971). For
Fig. 1. Map of São Paulo state and Satellite Image indicating the sampling sites in the region of Ribeira Valley and South Coast of São Paulo state, Brazil. Source: Atlas Biota and Google Earth.
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Table 1 General characteristics and location of the streams. Municipalities
a
Streams
Land use
Coordinates ◦
Width (m) ◦
Depth (cm)
Electric conductivity (S cm−1 )
Temp. (◦ C)
DO (mg L−1 )
Cajati
B1 B2
Banana cultivation Banana cultivation
S24 51 W48 05 S24◦ 50 W48◦ 14
1.50 1.27
7.0 4.0
b
na 1.50
22.7 21.2
7.80 10.30
Jacupiranga
B3 B4 B5
Banana cultivation Banana cultivation Banana cultivation
S24◦ 50 W48◦ 14 S24◦ 51 W48◦ 05 S24◦ 51 W48◦ 6
0.95 0.52 0.78
8.3 5.0 5.0
0.50 0.05 1.13
21.7 26.2 21.2
7.87 8.50 8.45
Cananéia
M1 M2 M3 M4 M5
Preserved Preserved Preserved Preserved Preserved
S24◦ 59 S25◦ 00 S24◦ 57 S24◦ 57 S24◦ 58
1.5 2.16 1.93 1.47 2.71
15.0 14.2 15.1 13.4 22.1
b
19.4 19.2 19.0 19.5 20.3
8.5 9.56 9.27 9.03 8.20
na 0.03 0.21 0.21 0.24
B = banana streams; M = preserved streams. na = not analyzed.
the data set (total EPTC of the 10 streams), a multivariate analysis of correspondence was applied to calculate the similarity between streams. The EPTC groups, which showed a close correlation, were identified and grouped to a further similarity test (ANOSIM). This test was used to detect significant differences between the two groups. For this analysis, 5% as p-level was considered. ANOSIM was calculated using Simpson as distance measure. The correspondence analysis and the ANOSIM were calculated by using the PAST Program (Version 1.68) (Hammer et al., 2001). We also applied a simple method to find indicator species characterizing groups of sites (preserved or disturbed). This analysis called indicator species analysis (ISA) (Dufrêne and Legendre, 1997), combines species relative abundance with its relative frequency of occurrence in the various groups of sites. This index is maximum when all individuals of a species are found in a single group of sites and when the species occurs in all sites of that group; it is a symmetric indicator. According to this technique, there are groups, in the data set, which can be indicated by some taxa. This analysis was made using the PC-ORD 4 (Mccune and Mefford, 1999) program and was validated by the Monte Carlo test, with 5000 permutations.
3. Results In total, 1812 individuals of EPTC were identified, in which 1105 organisms were in streams in areas of banana cultivation and 706 in preserved streams (Table 2). Heterelmis (Elmidae) was dominant in both sets of streams. Besides this, in preserved streams, Hexacylloepus (Elmidae), Tupiperla and Paragrypopteryx (Gripopterygidae) and Nectopsyche (Leptoceridae) also exhibited a notable presence. Leptonema (Hydropsychidae) and Xenelmis (Elmidae) were dominant in streams located in areas of banana cultivation (Table 2). The preserved streams had higher richness and diversity of EPTC than banana plantation streams. The main community characteristics are presented in Table 3. The correspondence analysis applied to the EPTC fauna delimited two groups: one grouping the assemblages in streams located in preserved areas (M1, M2, M3, M4 and M5) and the other one in streams in areas adjacent to banana plant cultivation (B1, B2, B3, B4 and B5) (Fig. 2). The test of similarity (ANOSIM) applied to the two groups, pointed to significant differences (p = 0.0083) between the situations. Dissolved oxygen (O2 ) also presented high concentrations in all streams with banana culture and in preserved areas. The values varied from 7.80 mg L−1 (B1 stream) to 10.30 mg L−1 (B2 stream), both located in areas with banana cultivation. Values of electric conductivity were slightly higher in areas with banana cultivation than preserved areas. The high value was detected for the B1 stream (0.03 S cm−1 ) and low value in M1 stream (1.50 S cm−1 ). The
1,6 1,2 0,8 0,4
Axis 2
a b
W48◦ 2 W48◦ 04 W48◦ 59 W48◦ 00 W48◦ 00
M4 M5 M2 M3 M1
B4
0
B5
B3
-0,4 -0,8 -1,2 -1,6 -2
B1 B2
-0,9 -0,6 -0,3
0
0,3
0,6
0,9
1,2
1,5
1,8
Axis 1 Fig. 2. Correspondence analysis applied for the EPTC species of the 10 streams. Legends as Table 1.
values of these components, as well as of the other measurements of physical and chemical characteristics, are presented in Table 1. The analyses of indicator species point to five species in preserved streams (Paragrypopteryx sp., Anacroneuria sp., Phylloicus sp., Triplectides sp. and Helicopsyche sp.) and two species in banana streams (Americabaetis sp. and Leptonema sp.) (Table 4). 4. Discussion Aquatic insects such as those in the EPTC orders known to be pollution-sensitive have been considered pertinent to use for stream classifications (Cayrou et al., 2000; Compin and Céréghino, 2003). According to these authors, EPTC is a good biological indicator of river quality, and it is also easy to measure since it is based on the only presence of species belonging to well-known groups of insects currently identified by specialists. The presence or the absence of many EPTC species whose ecology is well known (Vinc¸on and Thomas, 1987; Compin and Céréghino, 2003) could provide diagnostic clues when interpreting the score provided by the assessment method. In accordance with the researchers, in the field, only a qualitative sampling is required, thus the counting of sorted individuals is not necessary. By contrast, to verify the indicative value of taxa, quantitative samples are necessary. The five streams analyzed in banana areas had different distributions of EPTC species richness when compared to forested sites and the results also pointed to 7 species that would be used as indicator species from studied streams. So, our results justified the use of EPTC species indices for monitoring streams located in areas with
J.J. Corbi et al. / Ecological Indicators 25 (2013) 156–161
159
Table 2 EPTC taxa collected in preserved and banana streams. Legends as Table 1. Taxa/streams
B1
B2
B3
B4
B5
M1
M2
M3
M4
M5
Chrysomelidae sp. Curculionidae Dryopidae sp. Pelonomus sp. Austrolimnius sp. Cylloepus sp. Heterelmis sp. Hexacylloepus sp. Macrelmis sp. Xenelmis sp. Phanocerus sp. Promoresia sp. Hydraena sp. Berosus sp. Paracymus sp. Lutrochus sp. Ectopria sp. Psephenus sp. Scirtidae sp.1 Scirtidae sp.2 Scirtidae sp.3 Staphylinidae sp. Grypopteryx sp. Tupiperla sp. Paragrypopteryx sp. Anacroneuria sp. Kempnyia sp. Ephemeroptera sp. Caenis sp. Americabaetis sp. Baetodes sp. Paracloeodes sp. Cryptonympha sp. Campylocia sp. Traverhyphes sp. Askola sp. Farrodes sp. Hylister sp. Leptohyphes sp. Miroculis sp. Thraulodes sp. Atopsyche sp. Phylloicus sp. Austrotinodes sp. Hydropsychidae sp. Blepharopus sp. Leptonema sp. Leptonema aff. sp. Macronema sp. Metrichia sp. Ochrotrichia sp. Oxyethira sp. Protoptila sp. Atanatolica sp. Nectopsyche sp. Triplectides sp. Barypenthus sp. Marilia sp. Chimarra sp. Cernotina sp. Polyplectropus sp. Helicopsyche sp. Xiphocentron sp.
– – 31 – 24 – 213 2 – 149 – – – 1 13 – 2 2 – – – 4 – – – – – – – 2 – – – – – – – – – – – – – – – – 41 – – 45 – – – 1 1 – – – 1 – – – 1
– – 1 – 2 – 17 1 – 91 – – – – 1 – 1 – – – 1 – 1 – – – – – – 2 2 – – – – – – – – – – 1 – – – – 2 – – 6 – – – – – – – – 1 – – – –
– 1 2 1 – – 17 26 – – – – 1 – 7 – – – – – – – – – – – – – – 4 – – – – – – – – – – – – – – – – 13 – – 2 1 – – – – – – – – – – – –
1 3 – – – 1 3 3 – – – – – 34 – – – – – – – – – – – – – – 41 40 – 2 – – 63 – 3 – – 4 – – – – – 3 64 – – 5 1 4 – – – – – – – – – – –
– – – – – 1 20 1 – – – – 1 – – – – – 1 – – – – 1 – – – – – 3 3 – – – 31 – – – – 1 – 1 – – – – 21 2 – – – – 2 – – – – – – – – – –
– – 2 – – – 19 11 2 – – – – – – – 1 – – – – – – 14 2 – – – – – – – – – – – 2 – – 7 – – 2 – – – 1 – – – – – – 1 – 1 – – 1 – – 1 –
– – 5 – 1 1 21 11 11 8 3 1 – 1 3 2 – – 2 1 – – – – 1 21 13 – – 1 – – 1 3 2 – – 1 – – 4 – 5 – 1 2 4 – – – – – – – 54 5 7 1 – – – 5 –
2 – – – – – 24 13 – – – – – – – – – – 1 – – – – – 3 7 – 13 – – – – – 4 – 9 3 – – 16 – 1 – – – 2 11 1 3 2 1 – – 1 4 2 – 1 1 8 2 13 –
– – – – – – 14 8 – – – – – – – – – – 4 3 – – – 30 21 3 2 – 1 2 – – 3 – – 6 6 3 – 26 – 1 1 1 – 10 4 – 7 2 – – – 2 8 2 – – – – – 2 –
1 – – – – – 17 14 – – – – 1 6 – – – 2 – 2 1 – – 23 18 2 2 – – – – – – – – 3 – – 3 – – – 1 – 1 8 – 1 – – 1 – – – – 3 2 – – – – 3 –
different land uses. In the same way, the low EPTC taxonomic resolution used in the present study clearly gave important information about the indicator taxa in the streams, specially for Plecoptera (Paragrypopteryx sp. and Anacroneuria sp.) and Trichoptera (Phylloicus sp., Triplectides sp. and Helicopsyche sp.) in the preserved streams, and Trichoptera Leptonema sp. and Ephemeroptera Americabaetis sp. in the disturbed streams. Although Coleoptera have been, in some cases, considerably good indicators of disturbed environments such as, for example, urban runoff, chemical pollution
and regulated flow (Compin and Céréghino, 2003), in the present study, this group does not present indicative value. Our results also show the importance of riparian vegetation, which provided a higher EPTC taxa richness in the forested streams (M1–M5) when compared to the areas with banana cultivation (B1–B5). Some factors like pollution, riparian vegetation and stream order, could have influenced the species richness of the studied streams, as observed by Diniz-Filho et al. (1998) in the central region of Brazil (Goiás state) and by Corbi and Trivinho-Strixino
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Table 3 Main community characteristics for the EPTC fauna of the 10 streams. Legends as Table 1.
EPTC family richness %Ephemeroptera %Plecoptera %Trichoptera %Coleoptera %EPTC Individuals Dominance D Shannon H Margalef Equitability J
B1
B2
19 0.7 0 7.57 38.1 46.07 534 0.26 1.72 2.87 0.59
16 0.97 0.24 2.43 28.0 31.63 130 0.51 1.24 3.08 0.45
B3 14 1.63 0 6.91 23,0 31.56 77 0.19 1.99 2.99 0.75
B4
B5
M1
M2
M3
M4
M5
21 21.21 0 7.04 7.7 46.77 275 0.16 2.15 3.56 0.71
15 26.26 0.56 15.08 13.9 51.45 89 0.23 1.82 3.12 0.67
16 7.26 12.90 5.65 28.5 54.47 67 0.16 2.21 3.57 0.80
35 3.66 10.98 25.61 22.5 62.46 204 0.11 2.82 6.58 0.79
28 16.73 3.72 19.70 15.4 56.92 148 0.08 2.85 5.40 0.86
31 12.24 14.58 10.42 7.6 44.91 172 0.09 2.87 5.83 0.84
24 2.88 18.52 8.23 18.6 47.93 116 0.11 2.57 4.84 0.81
Table 4 Indicator species in preserved and banana streams. IV (%) species indicator values; p value obtained by 5000 permutations (Monte Carlo Test). Taxa
Stream
IV (%)
p
Paragrypopteryx sp. Anacroneuria sp. Americabaetis sp. Phylloicus sp. Leptonema sp. Triplectides sp. Helicopsyche sp.
Preserved Preserved Banana Preserved Banana Preserved Preserved
100.0 80.0 94.4 80.0 87.6 100.0 100.0
0.0080 0.0410 0.0220 0.0460 0.0470 0.0080 0.0080
(2008) in streams located in areas with sugarcane cultivation and pastures, without riparian vegetation (Cerrado areas in the state of São Paulo). The deforestation of riparian vegetation also appeared to be reflected in the high values of temperature observed in the water of the impacted streams (B1–B5). The higher temperature observed in the deforested streams compared to the preserved ones appeared to also reflect in the values of dissolved oxygen in the water measured. The concentrations of cations (Mg, Mn, Na, K) are the components that influence the values of electric conductivity of the streams. Results obtained for the values of electric conductivity, also appeared to be a reflection of agricultural activities. In the deforested streams located in agricultural areas, the input of fertilizers (N, P, K) containing metals as micronutrients, probably influenced the high values of this variable in the water as observed for streams located in areas with banana plant cultivation.
5. Conclusions These results show the potential use of EPTC invertebrate taxa for detect agriculture impacts, especially banana plant cultivation. In the present study, the application of species indicator method, as proposed by Dufrene and Legendre, gives precise and accurate information on EPTC species and discriminate seven indicator species. The species identification obtained here could also become useful for agriculture impact assessment. Furthermore, our results demonstrate the importance of the preservation of riparian vegetation for the EPTC community’s distribution, which appeared to be the most important factor influencing the composition of these aquatic fauna and are also responsible for absorption of toxic products which come from the neighboring cultivated areas.
Acknowledgements The authors gratefully acknowledge the fruitful suggestions of Professor Pedro P. Corbi and Dra. Vanessa Colombo Corbi. We thank the National Council for Scientific and Technological Development (CNPq), for a research fellowship.
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