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Hierarchical dynamics influence the distribution of immature black flies (Diptera: Simuliidae)
Acta Tropica 177 (2018) 105–115
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Hierarchical dynamics influence the distribution of immature black flies (Diptera: Simuliidae)
MARK
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Sankarappan Anbalagana, , Mani Kannana, Sundaram Dinakaranb, Chelliah Balasubramanianc, Muthukalingan Krishnand a
Department of Zoology, Government Arts College (Affiliated to Madurai Kamaraj University), Melur, 625106, Madurai, Tamil Nadu, India Department of Zoology, The Madura College, Madurai, 625011, Tamil Nadu, India c Department of Zoology & Microbiology, Thiagarajar College, Madurai, 625009, Tamil Nadu, India d Department of Biochemistry, School of Life Sciences, Central University of Rajasthan, Ajmer, 305817, Rajasthan, India b
A R T I C L E I N F O
A B S T R A C T
Keywords: Latitude Environmental variables Season Black fly Streams
Adult black flies (Simuliidae) are medically important insects and they are the sole vector of Onchocerca volvulus. Immature black flies are major components of aquatic macroinvertebrate assemblages in streams and play a vital role in nutrient dynamics. In this study, we examined effect of hierarchical dynamics (spatio-temporal pattern) on the distribution of immature black flies in South Indian streams. The sampling was done in streams of Western Ghats, South India. A total of 16 species belong to two subgenera: Simulium (10 species) and Gowmphostilbia (6 species) of Simulium were observed. Alpha diversity indices were analyzed, which indicate the abundance and species richness between sampling sites. Non-parametric analysis recognized the key environmental variables including latitude and stream order. Subsequently, the monsoon influences the larval assemblages and its association was high in leaf litter as revealed through statistical analyses. Although the members of the immature black fly assemblage with different environmental factors, they are very closely related to spatial and temporal organization and secondarily with other factors prevailing in streams.
1. Introduction In ecology, the behavior of a species living in precise environmental conditions is termed as ecological niche. Within this general framework, understanding the species delimit is challenging, because many species are not limited and they are distributed in different environments. In this context, assemblage pattern of a species is important to find the specific environmental variables related to the distribution of species. Increasing pollution of the world, relationship between environmental variables and species groups is obligatory and it is most significant if the species is a vector. Consequently, this study focused on the family Simuliidae of the order Diptera, are an important medical and veterinary group of small hematophagous insects. The adult female black fly bite causes large range of problems for humans and other vertebrates (Choochote et al., 2005). Black fly larvae play a vital role as principal processors of plant materials in streams due to its filter feeding organization (Malmqvist et al., 2004; Srisuka et al., 2015).
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The world black flies (Simuliidae) are represented by 2232 living species and 15 fossil species (Adler and Crosskey, 2017). In the Oriental region, black flies is represented by only one genus Simulium Latreille s. l. with ten subgenera (Currie and Adler 2008; Takaoka 2012). Of these, many species are recorded under vector groups. According to the world black fly inventory, the description of new species is increasing year by year. This may due two main reasons that taxonomic awareness/auxiliary concentration of this group and abundance of this species. Many reports suggesting the environmental factors play a major role for determining the distribution of black fly species (McCreadie et al., 2006a,b; Landeiro et al., 2009; Pachon and Walton, 2011; McCreadie and Adler, 2012; Rabha et al., 2013; Srisuka et al., 2015) and few reports reflecting that anthropogenic impacts influence the distributional pattern (Dinakaran and Anbalagan, 2007; Anbalagan et al., 2011, 2015). Still perplexing pattern found that assemblage of larval black fly species is related to whether environmental variables or anthropogenic impact.
Corresponding author. E-mail address: [email protected] (A. Sankarappan).
http://dx.doi.org/10.1016/j.actatropica.2017.09.030 Received 25 August 2017; Received in revised form 19 September 2017; Accepted 30 September 2017 Available online 07 October 2017 0001-706X/ © 2017 Elsevier B.V. All rights reserved.
Acta Tropica 177 (2018) 105–115
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Fig. 1. Map of Western Ghats in South India with sampling sites (sampling site’s name is given in Table 1).
South India contains the world’s eight ‘hottest hotspots’ of Western Ghats and covers 1600 km from Kanyakumari to the north of Mumbai. It is characterized by a diverse plant and animal communities and holds many mountainous streams, which are presumed to support the diversity of aquatic insects. Today, a large part of the forest areas of Western Ghats has been rehabilitated to agriculture and urbanization. With these impacts, forests have led to habitat destruction, increased fragmentation and human-wildlife conflict. At this situation, there is
necessary to study on the distribution and community structure of aquatic insects. The larval black flies are an important component in stream ecosystem, which heavily influenced by the alteration of environmental factors and anthropogenic impacts in streams of South India (Anbalagan et al., 2011). In this paper, we examined the two main aspects: the spatial and temporal distributional pattern of black flies and identify the precise environmental factor relating to the distribution of black flies in streams.
106
107
Manjalaru (11) Poolathur (12) Moolayar (13) Kurusedi (14) Silver cascade (15) Fairy falls (16)
Meenvallam (17) Kunthipuzha (18) Kallar (19) Barliar (20) Coonoor (21) Segur (22) Mavanalla (23) Cauvery river (24)
Palani hills Wildlife sanctuary
Nilgiri biosphere reserve
10°95′61” 11°02′95” 11°20′24” 11°20′71” 11°19′96” 11°30′57” 11°02′82” 12°44′80”
10°13′14” 10°16′15” 10°10′85” 10°13′28” 10°13′72” 10°13′52”
8°20′31” 8°23′75” 8°26′26” 8°33′95” 8°37′17” 8°42′19” 8°55′58” 8°57′49” 8°90′52” 8°96′88”
LAT (N)
76°54′16” 76°44′75” 76°52′91” 76°50′95” 76°48′51” 76°41′81” 76°40′68” 75°96′97”
77°37′30” 77°32′12” 77°36′72” 77°36′72” 77°31′95” 77°28′09”
77°32′14” 77°24′58” 77°31′53” 77°08′49” 77°24′75” 77°21′81” 77°14′18” 77°18′44” 77°05′81” 77°09′79”
LON (E)
145 72 343 385 1349 952 901 829
290 900 1075 1250 1590 2050
110 126 150 275 440 435 220 110 180 195
ELV (m)
3 3 4 3 2 3 2 4
4 2 3 2 3 2
3 4 3 3 3 3 4 2 4 4
STO
27 27 22 22 19 25 27 18
22 23 18 17 18 14
27 30 29 21 32 29 28 28 27 26
WAT (°C)
6.2 5.1 2.2 1.4 0.6 3.3 1.9 15
9.1 0.5 7.1 2.1 5.9 0.6
3.3 4.5 2.2 5.4 8.1 1.5 5.2 1.2 11.1 5.8
STW (m)
12 5 10 5 5 10 5 30
22 5 15 10 10 9
8 15 18 10 21 18 11 16 18 21
STD (cm)
0.02 0.01 0.05 0.05 0.04 0.01 0.15 0.01
0.03 0.06 0.05 0.10 0.05 0.09
0.01 0.01 0.35 0.13 0.01 0.01 0.05 0.01 0.04 0.06
CUV (s cm−1)
91 57 99 106 61 236 359 79
215 63 341 85 286 95
314 321 74 51 215 341 115 85 192 184
TDS (ppt)
10.4 9.8 8.4 8.2 7.4 10.1 8.1 11.2
11.4 9.2 10.4 9.8 12.3 8.2
11.2 7.3 9.8 11.2 10.5 9.2 12.1 8.5 8.3 9.2
DSO (mg L−1)
7.8 7.2 7.4 6.5 7.9 6.8 7.3 6.3
7.3 6.6 6.9 6.8 7.2 6.7
6.6 7.4 6.9 6.4 6.6 6.9 7.1 6.9 6.8 7.2
pH
126 94 112 145 86 334 506 111
111 65 124 41 265 74
234 85 254 116 36 47 102 38 51 286
CON (μsec)
61 48 55 172 42 155 237 65
56 29 65 26 75 34
116 48 124 53 17 22 45 26 30 21
SAL (ppm)
70 20 20 80 80 80 70 20
20 80 50 90 80 60
80 40 20 70 20 20 80 50 10 50
CAC (%)
7.5 6.0 6.8 7.5 6.1 6.1 4.0 6.1
6.4 7.4 7.6 7.3 6.1 7.5
5.7 6.3 6.3 6.2 7.5 8 7.3 6.4 7.0 7.0
SUI
Note: Lat: latitude, Long-longitude; ELV-elevation, STO-stream order, WAT-water temperature, STW-stream width, STD-stream depth, CUV-current velocity, TDS-total dissolved solids, DSO-dissolved oxygen, CON-conductivity, SAL-salinity, CACcanopy cover, SUI-substrate index; parentheses indicates site number.
Kuthirapanchan (1) Keeriparai (2) Nambiyar (3) Kottoor (4) Manimutharu (5) Agasthiar falls (6) Five falls (7) Chinnakuttalam (8) Kulathupuzha (9) Kallada river (10)
Agasthiar biosphere reserve
Stream name
Table 1 Physical and chemical parameters of sampling sites of South India.
A. Sankarappan et al.
Acta Tropica 177 (2018) 105–115
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Table 2 Abundance of black fly species in 24 sampling sites and the percentage of species occurrence.
sampling were done. The characteristic features of three sampling areas are as follows: Agasthiamalai biosphere reserve (ABR): This site lies between 8°8′–9°10′ North Latitude and 76°52′–77°34′ East Longitude. It comprises moist deciduous forest with many eco-tourist spots. Its stream has diversified substrates with the presence of anthropogenic impacts in many streams. From this region, 10 streams were sampled and month-wise sampling was done in Kulathupuzha river of ABR for a year. Nilgiri biosphere reserve (NBR): This biosphere lies between 10°50′N and 12°16′N latitude and 76°00′E–77°15′E longitude. This site encompasses three ecoregions: the moist deciduous forests, montane rainforests and dry deciduous forests. In this region, eight streams were selected and sampled. Its stream ranged from bedrock to sand bed and found anthropogenic impacts. Palani hills wildlife sanctuary (PWS): This area is located between latitude 10°7′N and 10°28′N and 77°16′E–77°46′E longitude. It comprises moist and dry deciduous forests. Its stream has a variety of stream substrates and tourist discharges. Six streams were sampled from this region (PWS).
Table 3 Diversity values for black fly larvae from 24 streams in South India. Site Number
Site Name
No. of taxa
Simpson index
Shannon index
Evenness
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24
Kuthirapanchan Keeriparai Nambiyar Kottoor Manimutharu Agasthiar falls Five falls Chinnakuttalam Kulathupuzha Kallada river Manjalaru Poolathur Moolayar Kurusedi Silver cascade Fairy falls Meenvallam Kunthipuzha Kallar Barliar Coonoor Segur Mavanalla Cauvery river
1 4 1 1 3 3 2 1 4 3 4 2 3 2 1 1 4 4 5 5 5 1 1 3
0 0.64 0 0 0.55 0.61 0.5 0 0.54 0.55 0.54 0.4 0.64 0.42 0 0 0.63 0.69 0.76 0.61 0.46 0 0 0.51
0 1.15 0 0 0.93 1 0.69 0 0.94 0.92 1.03 0.59 1.06 0.61 0 0 1.16 1.24 1.52 1.22 0.96 0 0 0.88
1 0.79 1 1 0.84 0.91 1 1 0.64 0.84 0.7 0.9 0.96 0.92 1 1 0.79 0.87 0.91 0.68 0.52 1 1 0.81
2.2. Sampling Overall, a total of 108 collections were carried out from 24 streams (3 collections/per site ×24 streams and 3 collections at fixed-stream sites ×12 months) between October 2013 and January 2016. Of 24 streams sampled, Kulathupuzha River was selected for studying temporal pattern due to abundance of larvae and easy access. Each stream was sampled from downstream to upstream (10 m), for approximately 2 h, by two research students. Larvae and pupae attached on aquatic substrates of bedrock, boulders, pebbles, leaves, woody debris and submerged human waste materials (polythene cover, snacks cover, cloths etc.) were collected hand using fine forceps. The collected larvae and pupae were preserved in 80% ethanol. The five to eight live pupae individually were kept alive in vials until emergence. After emergence, adult flies were kept alive in the same container for at least 12–24 h, in order to secure hardening and colouring of their body and legs. Adult flies, associated with their pupal exuviae, were used to confirm the species identification of the larvae (Srisuka et al., 2015). The adults, together with their pupal exuviae and cocoons were preserved in 80 %
2. Materials and methods 2.1. Study area The sampling areas were located in Western Ghats of South India (Fig. 1). Three major parts in Western Ghats were selected for sampling: (1) Agasthiamalai Biosphere reserve, (2) Nilgiri Biosphere reserve and (3) Palani hills wildlife sanctuary. In each sampling area, three replicate
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Table 4 Jaccard’s similarity index and beta diversity indices of larval black flies distributed in sampling sites. Sites
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
Jaccard’s index 1 1 0 2 1
1 0
0 0
0.33 0.17
0.33 0.4
0 0.2
0 0
0 0.17
0 0.33
0 0.2
0 0.17
0 0.2
0 0
0 0
0 0.6
0 0.33
0 0.5
0 0.29
0 0.13
0 0.25
0 0.25
0 0.17
1
0 1
0.33 0 1
0.33 0 0.5
0 0 0
0 0 0
0 0 0.2
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
1
0.25 1
0
0 0.14 0 0 0.17 0.17 0.5 0.25 1
0.2
0.17
0.25
0.2
0.25
0
0
0.17
0.17
0.14
0.14
0.14
0
0
0.2
0.67 0.33
0.2 0
0.33 0
0.25 0
0.33 0
0 0
0 0
0.2 0
0.2 0
0.17 0
0.17 0
0.17 0
0 0
0 0
0.25 0
0.75 1
0.14 0.17 1
0.2 0.25 0.5 1
0.17 0.2 0.75 0.67 1
0.2 0.25 0.5 1 0.67 1
0 0 0.25 0 0.33 0 1
0 0 0 0 0 0 0 1
0.14 0.17 0.33 0.2 0.17 0.2 0 0 1
0.33 0.17 0.33 0.2 0.17 0.2 0 0 0.33 1
0.13 0.14 0.29 0.17 0.14 0.17 0 0 0.5 0.5 1
0.13 0.14 0.13 0.17 0.14 0.17 0 0 0.5 0.29 0.67 1
0.13 0.14 0.5 0.4 0.6 0.4 0.2 0 0.13 0.29 0.43 0.43 1
0 0 0.25 0 0 0 0 0 0.25 0.25 0.2 0 0 1
0 0 0.25 0 0 0 0 0 0.25 0.25 0.2 0 0 1 1
0.17 0.2 0.17 0.25 0.2 0.25 0 0.33 0.17 0.17 0.14 0.14 0.14 0 0 1
3 4 5
1
6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Beta diversity indices Whittaker: Harrison: Cody: Routledge: Wilson-Shmida: Mourelle: Harrison 2: Williams:
0.5 1
5 0.33 45.5 0.61 11.4 0.76 0.04 0.38
–>
2.3. Data analysis
ethanol for identification at the subgenus, species-group or species level. The methods of collection and identification followed those of Takaoka (2003) and Adler et al. (2004). The following stream physicochemical parameters were measured at the time of each collection: stream depth, width, velocity, water temperature, pH, conductivity, dissolved oxygen, total dissolved solids and salinity. The values of temperature, pH, conductivity, total dissolved solids and salinity were taken using a portable water analysis tester (PCS Testr 35, Eutech instruments, India). Meter tape and steel ruler were used to measure stream width and depth, respectively, while a cork and a timer watch were used to measure stream velocity; the time taken for a cork to move one meter in distance. Stream substrates were classified according to Jowett et al. (1991). For each study site, the latitude and longitudinal coordinates were taken once and recorded using a hand held global positioning system (GPS) instrument (Garmin International Inc., Olathe, KS) and stream order identification in each study site followed by Harrel (1966).
The collected specimens were numerically counted and entered in MS-Excel sheet. These data was transformed to statistical software, PAST (v.3.16), where the data was analyzed. The diversity indices of Shannon–Wiener, Simpson, and Evenness were calculated. Similarities in species composition were calculated using Jaccard’s index based on a presence–absence matrix of the mosquito fauna. Beta diversity indices of Whittaker, Harrison, Cody, Routledge, Wilson–Shmida, Mourelle, and Harrison were estimated. The substrate index was calculated based on Suren (1996). The faunal structure with environmental variables among sampling sites and effect of seasonality on larval black fly distribution were subjected multivariate analyses of Canonical Correspondence Analysis (CCA) and Correspondence Analysis, respectively. Detrended Correspondence Analysis (DCA) was calculated to find the relationship between species and environmental variables. According to McCreadie et al. (2006a,b), the sampling statistics (t test, correlation coefficient (R2) and F test) were calculated to study the relationship
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Fig. 2. Correlation coefficient value between environmental factors and species richness.
Fig. 3. Triplot of Canonical correspondence analysis (CCA) for environmental variables in 24 streams.
order streams were carried out from three regions (ABR, NBR and PWS) of the study area. The physico-chemical parameters and streams substrates for 24 streams are given in Table 1. In total, 24,039 larvae belonging to 16 species and 2 subgenera (Simulium and Gomphostilbia) of Simulium were collected (Table 2). Of 16 species, 14 species were described and 2 species from each subgenus are not described. Among 16
between distribution of organism and the significant environmental variables showed by CCA and DCA results.
3. Results Of 24 streams, six second order, eleven third order and seven fourth
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Fig. 4. Detrended correspondence analysis (DCA) for species distribution and 24 sampling sites.
The 16 collected black fly species were statistically tested with the CCA highlighted environmental variables (Table 5). Consequently, Latitude were significantly related with six species (S. (S.) grisecens, S. (S.) gurneyae, S. (S.) nilgiricum, S. (S.) palniense, S. (S.) pattoni and S. (G.) cauveryense), stream order with five species (S. (S.) lineothorax, S. (S.) striatum, S. (S.) sp., S. (G.) peteri, S. (G.) takaokai), pH with two species (S. (S.) gravelyi and S. (S.) palmatum) and conductivity with two species (S. (G.) panagudiense and S. (G.) sp.) and S. (G.) kottoorense not related with these factors. For studying seasonal pattern of black fly distribution, Kulathupuzha River at ABR was selected for sampling. The physicochemical parameters of Kulathupuzha River for twelve months period are given in Table 6. A total of 7404 black fly larvae were collected under two subgenera Gomphostilbia and Simulium. Two species from Gomphostilbia (S. (G.) peteri and S. (G.) takaokai) and a species from Simulium (S. (S.) striatum) were identified. The larvae of Gomphostilbia were dominant (95%). S. (S.) striatum larvae were not considered for further analysis due to their petite distribution. Of 95% of Gomphostilbia immature, 40% of individuals account to leaf litter. Among the substratum, the leaf litter holds the higher number of larvae during sampling periods (Table 6). Black fly larvae were not found during May and June, due to dryness/summer. Overall, S. (G.) peteri was the dominant species, presenting density of 64% and they distributed in all stream substrates and, their maximum density was 36% in leaf litter followed by 26% in boulders, 14% in woody debris, 17% in bed rock and 6% in pebbles (Table 6). The highest percentage of S. (G.) peteri were observed in leaf litter during July (70%), in wood debris on December (24%), boulders and bed rock on April (43%, 25%) and in pebbles on December (14%). The larvae of S. (G.) takaokai showed a marked preference for leaf litter, with their distribution at higher number between December and February and
species, S. (S.) gravelyi (16%) and S. (S.) striatum (15.1%) were abundantly present. The most frequently distributed species was S. (S.) striatum (62.5%) followed by S. (G.) sp. (29.2%) and S. (S.) gurneyae (20.8%). Seven species: S. (S.) grisecens, S. (S.) palniense, S. (S.) palmatum, S. (S.) pattoni, S. (G.) takaokai, S. (G.) kottooresne and S. (G.) cauveryense were distributed between less than three streams. The highest diversity value was observed at site 19 (No. of taxa: 5; Shannon: 1.518; Simpson: 0.765) and eight sites (site number: 1, 3, 4, 8, 15, 16, 22, 23) had no diversity values, holding single taxa (Table 3). Among the distribution of black fly species in sampling sites of three regions, Five falls and Kallada River at ABR, Manjalaru and Moolayar at PWS and Kallar and Barliar at NBR had the highest similarity and other sites showed partial to low similarity revealed by the Jaccard’s similarity index. The same pattern was observed in the beta diversity indices (Table 4). Result of correlation coefficient analysis showed that the environmental variable of pH, stream order and latitude were interrelated with the distribution of taxa in streams than the other variables (Fig. 2). Further, for validating the above result, canonical correspondence analysis (CCA) was analyzed (Fig. 3). The eigen value and inter-site variability of CC-1 axis were 0.041 and 63.6% respectively. CCA result showed the latitude, stream order, pH and conductivity are significant variables for the distribution of black fly larvae. The result of Detrended correspondence analysis (DCA) was plotted in a scatter diagram (Fig. 4) and it shows the relationship between sites and species assemblages that sites 1 and 3 is closed with S. (G.) panagudiense followed by site 9 with S. (G.) takaokai, site 10 with S. (G.) peteri, site 4 with S. (G.) kottoorense, site 15 with S. (S.) gravelyi and site 16 with S. (S.) palniense. Based on the CCA result, the four environmental variables (pH, latitude, stream order and conductivity) were taken for further analysis to find the right factor responsible for species assemblage.
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Table 5 (continued)
Table 5 Statistical analysis between species (dependent) and environmental variables (independent) in 24 streams. Parenthesis-p value. Species
S. (S.) gravelyi
Statistical test
S. (S.) grisecens
S. (S.) lineothorax
S. (S.) striatum
S. (S.) gurneyae
S. (S.) palniense
S. (S.) pattoni
R2 F
0.08 0.72 (0.62)
t
0.96 (0.4)
S. (G.) peteri
S. (G.) takaokai
2
0.02 1.5 (0.23)
t
0.02 (0.9)
R2 F
0 1.8 (.16)
t
−0.24 (0.8)
R2 F
0 2.2 (0.1)
t
0.2 (0.8) 2
0.01 0.65 (0.6)
t
1.8 (0.01)
R2 F
0.15 1.7 (0.2)
t
1.11 (0.3)
R2 F
0.04 0.8 (0.5)
t
1.9 (0.1)
R F S. (S.) sp.
0.01 1.149 (0.37) 1.61 (0.1)
R F S. (S.) nilgiricum
2
t
R F S. (S.) palmatum
−0.14 (0.9)
t R F
Latitude
2
0.11 0.9 (0.4)
t
−1.71 (0.1)
R2 F
0.18 1.4 (0.2)
t
−1.51 (0.1)
R2 F
0.1 1.4 (0.3)
t
−0.86 (0.4)
R F
2
0.06 0.7 (0.5)
S. (G.) panagudiense
t
−2.26 (0.1)
R2 F
0.19 1.9 (0.9)
S. (G.) kottoorense
t
−0.99 (0.3)
R F S. (G.) cauveryense
2
3.34 (0.1)
t R F
0.06 0.6 (0.7)
2
0.19 3.76 (0.01)
pH
Stream order
Conductivity
0.79 (0.4) 0.03
−0.4 (0.7) 0
0.2 (0.9)
−0.41 (0.7) 0
0.55 (0.6) 0
0.1 (0.9)
1.22 (0.2) 0.08
2.1 (0.04) 0.13
−0.5 (0.6)
0.19 (0.9) 0
−0.1 (0.9) 0.04
−1.7 (0.1)
1.23 (0.2) 0.05
2.2 (0.04) 0.29
−0.8 (0.4)
−0.16 (0.8) 0
−1 (0.3) 0.01
−1 (0.4)
1.48 (0.2) 0.1
−0.8 (0.4) 0.06
−1 (0.3)
−1.26 (0.2) 0.07
−0.8 (0.4) 0.03
−0.8 (0.4)
−0.57 (0.5) 0
0.59 (0.6) 0
−0.1 (0.9)
0.58 (0.6) 0
0.99 (0.3) 0.04
−0.7 (0.5)
0.51 (0.6) 0.01
1.69 (0.1) 0.16
0.7 (0.5)
−0.36 (0.7) 0.01
1.2 (0.2) 0.11
−0.5 (0.6)
−0.84 (0.4) 0.04
0.07 (0.9) 0
1.9 (0.1)
−1.17 (0.3) 0.09
−0.3 (0.8) 0
−0 (0.9)
−2.7 (0.1) 0.12
2.12 (0.1) 0.07
−0.4 (0.7)
Species
Statistical test
Latitude
pH
Stream order
Conductivity
S. (G.) sp.
t
1.21 (0.2) 0.11 6.1 (0.001)
−0.8 (0.4) 0.04
4.7 (0.1)
R2 F
0.43 (0.7) 0.03
0.6
0 Bold-significant value.
0
July and August (Table 6). The highest percentage of association with stream substrates were: leaf litter on December (56%), woody debris on November and March (33%), bed rock on July (29%), boulders on November (31%) and pebbles on August (11%). Alpha diversity indices of Shannon and Simpson values were high (H: 1.49 ± 0.02, 1-D: 0.75 ± 0.06) between September and January. One-way ANOVA resulted that stream substrates were significantly (F = 5.502; P = 0.291) related with larval abundance. The effect of seasonality on two species distribution was analyzed individually by Correspondence Analysis (CA). In CA of S. (G.) peteri, eigen value of CA1 and CA2 axes were 0.043 and 0.029. Scatter plot based on CA axes score shows changes in black fly species among months (Fig. 5). CA result for S. (G.) peteri revealed that larval abundance was associated with leaf litter on July (Fig. 5). While, S. (G.) takaokai larval abundance was related to pebbles and boulders on October and their eigen value of CA1 and CA2 axes were 0.068 and 0.057.
0
0
0
0
0
4. Discussion The Oriental Region has the second largest black fly fauna than the other zoogeographical regions with 24% of the world total existing species. Of these, two subgenera Gompostilbia (37%) and Simulium (44%) consist of maximum number of species (Takaoka, 2017). Possibly, 16 species were collected under two subgenera Gomphostilbia and Simulium from 24 streams of three protected regions in South India. Among 16 species, 10 species were observed under the subgenus Simulium and rest of the species belongs to Gomphostilbia. Simulium (Simulium) striatum was common species and they distributed in more than 15 sampling streams and other species restrict to site specific or variation of environmental factors. Supportively, the distribution of black flies is influenced by the factors of breeding site characteristics, seasonal abundance, stream size and depth, food supply, substratum, velocity, light and physico-chemical conditions (Lake and Burger, 1983; McCreadie et al., 2006a; McCreadie et al., 2006b; McCreadie and Adler, 2012; Rabha et al., 2013). In this study, we observed that the three sampling sites (Moolayar and Silver cascade at PWS and Kunthipuzha at NBR) had the human discharges like sewage and solid wastes, whereas these sites hold many black fly larvae. However, other streams sites had less human impact and pristine streams with wide range of species distribution and black fly larvae were markedly different between sampling sites, as shown through beta diversity analysis. Hence, species richness was correlated with environmental variables by using CCA, suggesting that the four factors such as latitude, stream order, pH and conductivity were significantly related with larval assemblages. This outcome contradicts with the report of Figueiro et al. (2012) that leaf litter, rocky substrate, riparian vegetation and water velocity were significantly related with black fly assemblages and explained the
0
0
0.1
0
0
0.1
0
0
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Table 6 Physico-chemical parameters and abundance (%) of black fly larvae in five larval habitats of Kulathupuzha River (LL-Leaf litter, WD-Woody debris, BR-Bedrock, BO-Boulder, PE-Pebbles, n-total no. of larvae/12 months).
WAT (°C) STW (m) STD (cm) CUV (s cm−1) TDS (ppt) DSO (mg L−1) pH CON(μsec) SAL (ppm) CAC (5) SUI
Jan
Feb
Mar
Apr
May
Jun
Jul
Aug
Sep
Oct
Nov
Dec
26 5.8 21 0.06 184 9.2 7.2 286 21 50 7
25 5.4 20 0.07 195 9.1 7.3 296 22 50 7.1
27 4.9 19 0.1 210 8.9 7.5 302 25 50 7.3
28 4.1 18 0.2 190 8.2 7.2 278 20 45 7.4
0 0 0 0 0 0 0 0 0 0 0
29 3.1 12 0.05 185 8.8 7.2 212 23 50 7.9
27 4.3 15 0.05 170 9.1 7.2 235 24 50 7.3
25 5.2 20 0.05 160 9.5 7.2 254 24 50 7
25 5.8 20 0.02 180 10.3 7.3 241 25 50 7
23 6.1 25 0.01 190 9.6 7.3 256 25 50 7.5
21 7.5 26 0.01 160 9.8 7.4 278 22 50 7
20 7.1 25 0.05 175 10.1 7.3 281 22 50 6.9
S. (G.) peteri
LL WD BR BO PE n
38.8 10.3 12.9 31 6.9 7.3
37 10.9 18.1 29.7 4.35 8.7
40.8 12.7 14.8 31.7 0 8.9
16.7 15.3 25 43.1 0 4.5
0 0 0 0 0 0
0 0 0 0 0 0
70 0 16.7 6.67 6.67 1.9
34.6 21 17.3 25.9 1.23 5.1
33.3 18.5 15.6 19.3 13.3 8.5
27.5 17.3 20.7 26.4 8.14 18.6
30.4 17.8 16.8 24.8 10.2 19
27.7 24 10.3 24 14 17
S. (G.) takaokai
LL WD BR BO PE n
44.4 30.2 12.7 11.1 1.59 7.18
50 23.9 12.5 10.2 3.41 11
38.5 32.5 16 9.47 3.55 20
0 0 0 0 0 0
0 0 0 0 0 0
0 0 0 0 0 0
50 0 29.2 18.8 2.08 5.5
50.7 16.4 0 21.9 11 8.3
31.6 29.3 14.9 14.4 9.77 20
33.3 25.8 9.09 24.2 7.58 7.52
15.4 32.7 11.5 30.8 9.62 8.3
56 22 13.8 6.42 1.83 12.4
Note: WAT-water temperature, STW-stream width, STD-stream depth, CUV-current velocity, TDS-total dissolved solids, DSO-dissolved oxygen, CON-conductivity, SAL-salinity, CACcanopy cover, SUI-substrate index.
deeper (Pramual and Wongpakam, 2010). The seasonal pattern of the present study revealed that larval assemblages were peak in rainy seasons (South-west monsoon and North-east monsoon). The black fly larvae were highly associated with leaf litter than the other stream substrates. During south-west monsoon, the larvae of S. (G.) peteri were highly associated with leaf litter, whereas, S. (G.) takaokai association in north-east monsoon. The stream substrates of bedrock, boulders, stones and plant matter influence on the distribution of benthic fauna (Oliveira et al., 2014). Of these, plant material accumulated in streambeds promotes spatial heterogeneity, food and shelter for aquatic invertebrates (Carvalho and Uieda, 2010). This study illustrates the importance of spatio-temporal organization for determining the distribution of black fly in streams. Latitude, stream order, water pollution, water conductivity are the most important factors influencing species assemblages. The higher number of distribution was found in rainy season with leaf litter substratum. In particular, the present study highlights the spatial and temporal variations are the prime factor and act synergistic on the distribution of black flies as per the hierarchical structure obtained whereas as the anthropogenic impact is known to be a successive factor and works independently. Future research should be directed to conduct long-term data to track the response of black fly communities to environmental and climate change in streams.
competitive pressures in each microhabitat of sampling site determine the distribution of species. The CCA suggested the five significant factors were statistically tested to find the species specific relationship. Consequently, latitude and stream order related with eleven species, and conductivity and pH each with two species. The abundant black fly species of S. ochraceum and S. paynei, showed the spatial separation with substrates and altitudes and larval black fly distribution varied with environmental variables including stream size (Grillet and Barrera, 1997). In this study, latitude and stream order influence the population dynamics and community structure of many black fly species in South Indian streams, it supported by the following observations: physical characteristics of streams (McCreadie et al., 1995), physicochemical variables (McCreadie and Colbo, 1992), and biotic interactions (Hart, 1987). The close relationship between aquatic insect life cycle traits and spatial heterogeneity degree conferred ecological importance at the small scale level (Scarsbrook and Townsend, 1993) due to variability of stream substrates and heterogeneous environments (Resh et al., 1988). The improved precipitation would be enhanced dispersal of black fly larvae due to heavy water flow (Matthiessen et al., 2010). The marked differences were found in the distribution of black fly larvae between the dry and rainy seasons; however, species richness was significantly higher in the rainy season, when rivers are faster and
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Fig. 5. Correspondence Analysis representing the distribution of black fly larvae and seasonality in first and second axes in Kulathupuzha River of Southern Western Ghats.
Anbalagan, S., Pandiarajan, J., Dinakaran, S., Krishnan, M., 2011. Effect of tourism on the distribution of larval blackflies (Diptera: Simulium) in Palni hills of South India. Acta Hydrobiol. Sin. 35 (4), 688–692. Anbalagan, S., Balachandran, C., Arunprasanna, V., Kannan, M., Dinakaran, S., Krishnan, M., 2015. A new species of Simulium (Gomphostilbia) (Diptera: Simuliidae) from South India, with keys to Indian members of the subgenus Gomphostilbia. Zootaxa 3974 (4), 555–563. Carvalho, E.M., Uieda, V.S., 2010. Input of litter in deforested and forested areas of a tropical headstream. Braz. J. Biol. 70 (2), 283–288. Choochote, W., Takaoka, H., Fukuda, M., Otsuka, Y., Aoki, C., Eshima, N., 2005. Seasonal abundance and daily flying activity of black flies (Diptera Simuliidae) attracted to human baits in Doi Inthanon National Park, Northern Thailand. Med. Entomol. Zool. 56, 335–348. Currie, D.C., Adler, P.H., 2008. Global diversity of black flies (Diptera: Simuliidae) in freshwater. Hydrobiologia 595, 469–475. Dinakaran, S., Anbalagan, S., 2007. Anthropogenic impacts on aquatic insects in six
Acknowledgement This research was supported by a grant from the Science and Engineering Research (SERB), New Delhi India (Ref. No: SB/FT/LS102/2012 and ECR/2016/000191). References Adler, P.H., Crosskey, R.W., 2017. World Blackflies (Diptera: Simuliidae): a Comprehensive Revision of the Taxonomic and Geographical Inventory [2017]. Available from http://www.clemson.edu/cafls/biomia/pdfs/blackflyinventory.pdf. Adler, P.H., Currie, D.C., Wood, D.M., 2004. The Black Flies (Simuliidae) of North America. Cornell University Press, Ithaca.
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A. Sankarappan et al. streams of southern western ghats. J. Insect Sci. 7 (37), 1–9. Figueiro, R., Gil-Azevedo, L.H., Maia-Herzog, M., Monteiro, R.F., 2012. Diversity and microdistribution of black fly (Diptera: Simuliidae) assemblages in the tropical savanna streams of the Brazilian cerrado. Mem. Inst. Oswaldo Cruz. 107, 362–369. Grillet, M.E., Barrera, R., 1997. Spatial and temporal abundance, substrate partitioning and species co-occurrence in a guild of neotropical blackflies (Diptera: Simuliidae). Hydrobiologia 345, 197–208. Harrel, R.C., 1966. Stream Order and Community Structure of Benthic Macroinvertebrates and Fishes in an Intermittent Stream. Oklahoma State University, USA, pp. 6–11 (Ph.D. thesis). Hart, D., 1987. Processes and patterns of competition in larval black flies. In: Kim, K.C., Merritt, R.W. (Eds.), Black Flies: Ecology, Population Management and Annotated World List. Pennsylvania State University, University Park, pp. 109–128. Jowett, I.G., Richardson, J., Biggs, B.J.F., Hickey, C., Quinn, J.M., 1991. Microhabitat preferences of benthic invertebrates and the development of generalised Deleatidium spp. habitat suitability curves, applied to four New Zealand rivers. N. Z. J. Mar. Freshwater Res. 25, 187–199. Lake, D.J., Burger, J.F., 1983. Larval distribution and succession of outlet breeding blackflies (Diptera: simuliidae) in New Hampshire. Can. J. Zool. 61, 2519–2533. Landeiro, V.L., Pepinelli, M., Hamada, N., 2009. Species richness and distribution of black flies (Diptera Simuliidae) in the Chapada Diamantina region, Bahia Brazil. Neotrop. Entomol. 38, 332–339. Malmqvist, B., Adler, P.H., Kuusela, K., Merritt, R.W., Wotton, R.S., 2004. Black flies in the boreal biome, key organisms in both terrestrial and aquatic environments: a review. Ecoscience 11, 187–200. Matthiessen, B., Mielke, E., Sommer, U., 2010. Dispersal decreases diversity in heterogeneous metacommunities by enhancing regional competition. Ecology 91, 2022–2033. McCreadie, J.W., Adler, P.H., 2012. The roles of abiotic factors, dispersal, and species interactions in structuring stream assemblages of black flies (Diptera: Simuliidae). Aquat. Biosyst. 8 (14), 1–11. McCreadie, J., Colbo, M.H., 1992. Spatial distribution patterns of larval cytotypes of the Simulium venustum/verecundumcomplex on the Avalon Peninsula, Newfoundland: factors associated with cytotype abundance and composition. Can. J. Zool. 70, 1389–1396. McCreadie, J., Adler, P.H., Colbo, M.H., 1995. Community structure of larva black flies (Diptera: Simuliidae) from the Avalon peninsula, Newfoundland. Ann. Ent. Soc. Am.
88, 51–57. McCreadie, J.W., Adler, P.H., Grillet, M.E., Hamada, N., 2006a. Sampling and statistics in understanding distributions of black fly larvae (diptera: simuliidae). Acta Entomol. Serb. 89–96. McCreadie, J.W., Adler, P.H., Hamada, N., Grillet, M.E., 2006b. Sampling and statistics in understanding distributions of black fly larvae (Diptera: Simuliidae). Acta Entomol. Serb. 89–96. Oliveira, V.C., Goncalves, E.A., Alves, R.G., 2014. Colonization of leaf litter by aquatic invertebrates in an Atlantic Forest stream. Braz. J. Biol. 74 (2), 267–273. Pachon, R.T., Walton, W.E., 2011. Seasonal occurrence of black flies (Diptera: Simuliidae) in a desert stream receiving trout farm effluent. J. Vect. Ecol. 36, 187–196. Pramual, P., Wongpakam, K., 2010. Seasonal variation of black fly (Diptera: Simuliidae) species diversity and community structure in tropical streams of Thailand. Entomol. Sci. 13, 17–28. Rabha, B., Dhiman, S., Yadav, K., Hazarika, S., Bhola, R.K., Veer, V., 2013. Influence of water physicochemical characteristics on Simuliidae (Diptera) prevalence in some streams of Meghalaya India. J. Vector Borne Dis. 50, 18–23. Resh, V.R., Brown, A.V., Covich, A., Gurtz, M.E., Li, H.W., Minshall, G.W., Reice, S., Sheldon, A.L., Wallace, J.B., Wissmar, R.C., 1988. The role of disturbance in stream ecology. J. N. Am. Benthol. Soc. 7, 433–455. Scarsbrook, M.R., Townsend, C.R., 1993. Stream community structure in relation to spatial and temporal variation: a habitat templet study of two contrasting New Zealand streams. Freshw. Biol. 29, 395–410. Srisuka, W., Takaoka, H., Otsuka, Y., Fukuda, M., Thongsahuan, S., Taai, K., Choochote, W., Saeung, A., 2015. Seasonal biodiversity of black flies (Diptera: Simuliidae) and evaluation of ecological factors influencing species distribution at Doi Pha Hom Pok National Park, Thailand. Acta Trop. 149, 212–219. Suren, A.M., 1996. Bryophyte distribution patterns in relation to macro-, meso-, and microscale variables in South Island, New Zealand streams. New Zealand J. Mar. Freshwat. Res. 30, 501–523. Takaoka, H., 2003. The Black Flies (Diptera: Simuliidae) of Sulawesi, Maluku and Irian Jaya 22. Kyushu University Press, Fukuoka, pp. 581. Takaoka, H., 2012. Morphotaxonomic revision of simulium (Gomphostilbia) (Diptera: Simuliidae) in the oriental region. Zootaxa 3577, 1–42. Takaoka, H., 2017. Speciation, faunal affinities and geographical dispersal of black flies (Diptera: Simuliidae) in the oriental region. Acta Trop. 166, 234–240.
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Hierarchical dynamics influence the distribution of immature black flies (Diptera: Simuliidae)
MARK
⁎
Sankarappan Anbalagana, , Mani Kannana, Sundaram Dinakaranb, Chelliah Balasubramanianc, Muthukalingan Krishnand a
Department of Zoology, Government Arts College (Affiliated to Madurai Kamaraj University), Melur, 625106, Madurai, Tamil Nadu, India Department of Zoology, The Madura College, Madurai, 625011, Tamil Nadu, India c Department of Zoology & Microbiology, Thiagarajar College, Madurai, 625009, Tamil Nadu, India d Department of Biochemistry, School of Life Sciences, Central University of Rajasthan, Ajmer, 305817, Rajasthan, India b
A R T I C L E I N F O
A B S T R A C T
Keywords: Latitude Environmental variables Season Black fly Streams
Adult black flies (Simuliidae) are medically important insects and they are the sole vector of Onchocerca volvulus. Immature black flies are major components of aquatic macroinvertebrate assemblages in streams and play a vital role in nutrient dynamics. In this study, we examined effect of hierarchical dynamics (spatio-temporal pattern) on the distribution of immature black flies in South Indian streams. The sampling was done in streams of Western Ghats, South India. A total of 16 species belong to two subgenera: Simulium (10 species) and Gowmphostilbia (6 species) of Simulium were observed. Alpha diversity indices were analyzed, which indicate the abundance and species richness between sampling sites. Non-parametric analysis recognized the key environmental variables including latitude and stream order. Subsequently, the monsoon influences the larval assemblages and its association was high in leaf litter as revealed through statistical analyses. Although the members of the immature black fly assemblage with different environmental factors, they are very closely related to spatial and temporal organization and secondarily with other factors prevailing in streams.
1. Introduction In ecology, the behavior of a species living in precise environmental conditions is termed as ecological niche. Within this general framework, understanding the species delimit is challenging, because many species are not limited and they are distributed in different environments. In this context, assemblage pattern of a species is important to find the specific environmental variables related to the distribution of species. Increasing pollution of the world, relationship between environmental variables and species groups is obligatory and it is most significant if the species is a vector. Consequently, this study focused on the family Simuliidae of the order Diptera, are an important medical and veterinary group of small hematophagous insects. The adult female black fly bite causes large range of problems for humans and other vertebrates (Choochote et al., 2005). Black fly larvae play a vital role as principal processors of plant materials in streams due to its filter feeding organization (Malmqvist et al., 2004; Srisuka et al., 2015).
⁎
The world black flies (Simuliidae) are represented by 2232 living species and 15 fossil species (Adler and Crosskey, 2017). In the Oriental region, black flies is represented by only one genus Simulium Latreille s. l. with ten subgenera (Currie and Adler 2008; Takaoka 2012). Of these, many species are recorded under vector groups. According to the world black fly inventory, the description of new species is increasing year by year. This may due two main reasons that taxonomic awareness/auxiliary concentration of this group and abundance of this species. Many reports suggesting the environmental factors play a major role for determining the distribution of black fly species (McCreadie et al., 2006a,b; Landeiro et al., 2009; Pachon and Walton, 2011; McCreadie and Adler, 2012; Rabha et al., 2013; Srisuka et al., 2015) and few reports reflecting that anthropogenic impacts influence the distributional pattern (Dinakaran and Anbalagan, 2007; Anbalagan et al., 2011, 2015). Still perplexing pattern found that assemblage of larval black fly species is related to whether environmental variables or anthropogenic impact.
Corresponding author. E-mail address: [email protected] (A. Sankarappan).
http://dx.doi.org/10.1016/j.actatropica.2017.09.030 Received 25 August 2017; Received in revised form 19 September 2017; Accepted 30 September 2017 Available online 07 October 2017 0001-706X/ © 2017 Elsevier B.V. All rights reserved.
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Fig. 1. Map of Western Ghats in South India with sampling sites (sampling site’s name is given in Table 1).
South India contains the world’s eight ‘hottest hotspots’ of Western Ghats and covers 1600 km from Kanyakumari to the north of Mumbai. It is characterized by a diverse plant and animal communities and holds many mountainous streams, which are presumed to support the diversity of aquatic insects. Today, a large part of the forest areas of Western Ghats has been rehabilitated to agriculture and urbanization. With these impacts, forests have led to habitat destruction, increased fragmentation and human-wildlife conflict. At this situation, there is
necessary to study on the distribution and community structure of aquatic insects. The larval black flies are an important component in stream ecosystem, which heavily influenced by the alteration of environmental factors and anthropogenic impacts in streams of South India (Anbalagan et al., 2011). In this paper, we examined the two main aspects: the spatial and temporal distributional pattern of black flies and identify the precise environmental factor relating to the distribution of black flies in streams.
106
107
Manjalaru (11) Poolathur (12) Moolayar (13) Kurusedi (14) Silver cascade (15) Fairy falls (16)
Meenvallam (17) Kunthipuzha (18) Kallar (19) Barliar (20) Coonoor (21) Segur (22) Mavanalla (23) Cauvery river (24)
Palani hills Wildlife sanctuary
Nilgiri biosphere reserve
10°95′61” 11°02′95” 11°20′24” 11°20′71” 11°19′96” 11°30′57” 11°02′82” 12°44′80”
10°13′14” 10°16′15” 10°10′85” 10°13′28” 10°13′72” 10°13′52”
8°20′31” 8°23′75” 8°26′26” 8°33′95” 8°37′17” 8°42′19” 8°55′58” 8°57′49” 8°90′52” 8°96′88”
LAT (N)
76°54′16” 76°44′75” 76°52′91” 76°50′95” 76°48′51” 76°41′81” 76°40′68” 75°96′97”
77°37′30” 77°32′12” 77°36′72” 77°36′72” 77°31′95” 77°28′09”
77°32′14” 77°24′58” 77°31′53” 77°08′49” 77°24′75” 77°21′81” 77°14′18” 77°18′44” 77°05′81” 77°09′79”
LON (E)
145 72 343 385 1349 952 901 829
290 900 1075 1250 1590 2050
110 126 150 275 440 435 220 110 180 195
ELV (m)
3 3 4 3 2 3 2 4
4 2 3 2 3 2
3 4 3 3 3 3 4 2 4 4
STO
27 27 22 22 19 25 27 18
22 23 18 17 18 14
27 30 29 21 32 29 28 28 27 26
WAT (°C)
6.2 5.1 2.2 1.4 0.6 3.3 1.9 15
9.1 0.5 7.1 2.1 5.9 0.6
3.3 4.5 2.2 5.4 8.1 1.5 5.2 1.2 11.1 5.8
STW (m)
12 5 10 5 5 10 5 30
22 5 15 10 10 9
8 15 18 10 21 18 11 16 18 21
STD (cm)
0.02 0.01 0.05 0.05 0.04 0.01 0.15 0.01
0.03 0.06 0.05 0.10 0.05 0.09
0.01 0.01 0.35 0.13 0.01 0.01 0.05 0.01 0.04 0.06
CUV (s cm−1)
91 57 99 106 61 236 359 79
215 63 341 85 286 95
314 321 74 51 215 341 115 85 192 184
TDS (ppt)
10.4 9.8 8.4 8.2 7.4 10.1 8.1 11.2
11.4 9.2 10.4 9.8 12.3 8.2
11.2 7.3 9.8 11.2 10.5 9.2 12.1 8.5 8.3 9.2
DSO (mg L−1)
7.8 7.2 7.4 6.5 7.9 6.8 7.3 6.3
7.3 6.6 6.9 6.8 7.2 6.7
6.6 7.4 6.9 6.4 6.6 6.9 7.1 6.9 6.8 7.2
pH
126 94 112 145 86 334 506 111
111 65 124 41 265 74
234 85 254 116 36 47 102 38 51 286
CON (μsec)
61 48 55 172 42 155 237 65
56 29 65 26 75 34
116 48 124 53 17 22 45 26 30 21
SAL (ppm)
70 20 20 80 80 80 70 20
20 80 50 90 80 60
80 40 20 70 20 20 80 50 10 50
CAC (%)
7.5 6.0 6.8 7.5 6.1 6.1 4.0 6.1
6.4 7.4 7.6 7.3 6.1 7.5
5.7 6.3 6.3 6.2 7.5 8 7.3 6.4 7.0 7.0
SUI
Note: Lat: latitude, Long-longitude; ELV-elevation, STO-stream order, WAT-water temperature, STW-stream width, STD-stream depth, CUV-current velocity, TDS-total dissolved solids, DSO-dissolved oxygen, CON-conductivity, SAL-salinity, CACcanopy cover, SUI-substrate index; parentheses indicates site number.
Kuthirapanchan (1) Keeriparai (2) Nambiyar (3) Kottoor (4) Manimutharu (5) Agasthiar falls (6) Five falls (7) Chinnakuttalam (8) Kulathupuzha (9) Kallada river (10)
Agasthiar biosphere reserve
Stream name
Table 1 Physical and chemical parameters of sampling sites of South India.
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Table 2 Abundance of black fly species in 24 sampling sites and the percentage of species occurrence.
sampling were done. The characteristic features of three sampling areas are as follows: Agasthiamalai biosphere reserve (ABR): This site lies between 8°8′–9°10′ North Latitude and 76°52′–77°34′ East Longitude. It comprises moist deciduous forest with many eco-tourist spots. Its stream has diversified substrates with the presence of anthropogenic impacts in many streams. From this region, 10 streams were sampled and month-wise sampling was done in Kulathupuzha river of ABR for a year. Nilgiri biosphere reserve (NBR): This biosphere lies between 10°50′N and 12°16′N latitude and 76°00′E–77°15′E longitude. This site encompasses three ecoregions: the moist deciduous forests, montane rainforests and dry deciduous forests. In this region, eight streams were selected and sampled. Its stream ranged from bedrock to sand bed and found anthropogenic impacts. Palani hills wildlife sanctuary (PWS): This area is located between latitude 10°7′N and 10°28′N and 77°16′E–77°46′E longitude. It comprises moist and dry deciduous forests. Its stream has a variety of stream substrates and tourist discharges. Six streams were sampled from this region (PWS).
Table 3 Diversity values for black fly larvae from 24 streams in South India. Site Number
Site Name
No. of taxa
Simpson index
Shannon index
Evenness
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24
Kuthirapanchan Keeriparai Nambiyar Kottoor Manimutharu Agasthiar falls Five falls Chinnakuttalam Kulathupuzha Kallada river Manjalaru Poolathur Moolayar Kurusedi Silver cascade Fairy falls Meenvallam Kunthipuzha Kallar Barliar Coonoor Segur Mavanalla Cauvery river
1 4 1 1 3 3 2 1 4 3 4 2 3 2 1 1 4 4 5 5 5 1 1 3
0 0.64 0 0 0.55 0.61 0.5 0 0.54 0.55 0.54 0.4 0.64 0.42 0 0 0.63 0.69 0.76 0.61 0.46 0 0 0.51
0 1.15 0 0 0.93 1 0.69 0 0.94 0.92 1.03 0.59 1.06 0.61 0 0 1.16 1.24 1.52 1.22 0.96 0 0 0.88
1 0.79 1 1 0.84 0.91 1 1 0.64 0.84 0.7 0.9 0.96 0.92 1 1 0.79 0.87 0.91 0.68 0.52 1 1 0.81
2.2. Sampling Overall, a total of 108 collections were carried out from 24 streams (3 collections/per site ×24 streams and 3 collections at fixed-stream sites ×12 months) between October 2013 and January 2016. Of 24 streams sampled, Kulathupuzha River was selected for studying temporal pattern due to abundance of larvae and easy access. Each stream was sampled from downstream to upstream (10 m), for approximately 2 h, by two research students. Larvae and pupae attached on aquatic substrates of bedrock, boulders, pebbles, leaves, woody debris and submerged human waste materials (polythene cover, snacks cover, cloths etc.) were collected hand using fine forceps. The collected larvae and pupae were preserved in 80% ethanol. The five to eight live pupae individually were kept alive in vials until emergence. After emergence, adult flies were kept alive in the same container for at least 12–24 h, in order to secure hardening and colouring of their body and legs. Adult flies, associated with their pupal exuviae, were used to confirm the species identification of the larvae (Srisuka et al., 2015). The adults, together with their pupal exuviae and cocoons were preserved in 80 %
2. Materials and methods 2.1. Study area The sampling areas were located in Western Ghats of South India (Fig. 1). Three major parts in Western Ghats were selected for sampling: (1) Agasthiamalai Biosphere reserve, (2) Nilgiri Biosphere reserve and (3) Palani hills wildlife sanctuary. In each sampling area, three replicate
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Table 4 Jaccard’s similarity index and beta diversity indices of larval black flies distributed in sampling sites. Sites
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
Jaccard’s index 1 1 0 2 1
1 0
0 0
0.33 0.17
0.33 0.4
0 0.2
0 0
0 0.17
0 0.33
0 0.2
0 0.17
0 0.2
0 0
0 0
0 0.6
0 0.33
0 0.5
0 0.29
0 0.13
0 0.25
0 0.25
0 0.17
1
0 1
0.33 0 1
0.33 0 0.5
0 0 0
0 0 0
0 0 0.2
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
0 0 0
1
0.25 1
0
0 0.14 0 0 0.17 0.17 0.5 0.25 1
0.2
0.17
0.25
0.2
0.25
0
0
0.17
0.17
0.14
0.14
0.14
0
0
0.2
0.67 0.33
0.2 0
0.33 0
0.25 0
0.33 0
0 0
0 0
0.2 0
0.2 0
0.17 0
0.17 0
0.17 0
0 0
0 0
0.25 0
0.75 1
0.14 0.17 1
0.2 0.25 0.5 1
0.17 0.2 0.75 0.67 1
0.2 0.25 0.5 1 0.67 1
0 0 0.25 0 0.33 0 1
0 0 0 0 0 0 0 1
0.14 0.17 0.33 0.2 0.17 0.2 0 0 1
0.33 0.17 0.33 0.2 0.17 0.2 0 0 0.33 1
0.13 0.14 0.29 0.17 0.14 0.17 0 0 0.5 0.5 1
0.13 0.14 0.13 0.17 0.14 0.17 0 0 0.5 0.29 0.67 1
0.13 0.14 0.5 0.4 0.6 0.4 0.2 0 0.13 0.29 0.43 0.43 1
0 0 0.25 0 0 0 0 0 0.25 0.25 0.2 0 0 1
0 0 0.25 0 0 0 0 0 0.25 0.25 0.2 0 0 1 1
0.17 0.2 0.17 0.25 0.2 0.25 0 0.33 0.17 0.17 0.14 0.14 0.14 0 0 1
3 4 5
1
6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 Beta diversity indices Whittaker: Harrison: Cody: Routledge: Wilson-Shmida: Mourelle: Harrison 2: Williams:
0.5 1
5 0.33 45.5 0.61 11.4 0.76 0.04 0.38
–>
2.3. Data analysis
ethanol for identification at the subgenus, species-group or species level. The methods of collection and identification followed those of Takaoka (2003) and Adler et al. (2004). The following stream physicochemical parameters were measured at the time of each collection: stream depth, width, velocity, water temperature, pH, conductivity, dissolved oxygen, total dissolved solids and salinity. The values of temperature, pH, conductivity, total dissolved solids and salinity were taken using a portable water analysis tester (PCS Testr 35, Eutech instruments, India). Meter tape and steel ruler were used to measure stream width and depth, respectively, while a cork and a timer watch were used to measure stream velocity; the time taken for a cork to move one meter in distance. Stream substrates were classified according to Jowett et al. (1991). For each study site, the latitude and longitudinal coordinates were taken once and recorded using a hand held global positioning system (GPS) instrument (Garmin International Inc., Olathe, KS) and stream order identification in each study site followed by Harrel (1966).
The collected specimens were numerically counted and entered in MS-Excel sheet. These data was transformed to statistical software, PAST (v.3.16), where the data was analyzed. The diversity indices of Shannon–Wiener, Simpson, and Evenness were calculated. Similarities in species composition were calculated using Jaccard’s index based on a presence–absence matrix of the mosquito fauna. Beta diversity indices of Whittaker, Harrison, Cody, Routledge, Wilson–Shmida, Mourelle, and Harrison were estimated. The substrate index was calculated based on Suren (1996). The faunal structure with environmental variables among sampling sites and effect of seasonality on larval black fly distribution were subjected multivariate analyses of Canonical Correspondence Analysis (CCA) and Correspondence Analysis, respectively. Detrended Correspondence Analysis (DCA) was calculated to find the relationship between species and environmental variables. According to McCreadie et al. (2006a,b), the sampling statistics (t test, correlation coefficient (R2) and F test) were calculated to study the relationship
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Fig. 2. Correlation coefficient value between environmental factors and species richness.
Fig. 3. Triplot of Canonical correspondence analysis (CCA) for environmental variables in 24 streams.
order streams were carried out from three regions (ABR, NBR and PWS) of the study area. The physico-chemical parameters and streams substrates for 24 streams are given in Table 1. In total, 24,039 larvae belonging to 16 species and 2 subgenera (Simulium and Gomphostilbia) of Simulium were collected (Table 2). Of 16 species, 14 species were described and 2 species from each subgenus are not described. Among 16
between distribution of organism and the significant environmental variables showed by CCA and DCA results.
3. Results Of 24 streams, six second order, eleven third order and seven fourth
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Fig. 4. Detrended correspondence analysis (DCA) for species distribution and 24 sampling sites.
The 16 collected black fly species were statistically tested with the CCA highlighted environmental variables (Table 5). Consequently, Latitude were significantly related with six species (S. (S.) grisecens, S. (S.) gurneyae, S. (S.) nilgiricum, S. (S.) palniense, S. (S.) pattoni and S. (G.) cauveryense), stream order with five species (S. (S.) lineothorax, S. (S.) striatum, S. (S.) sp., S. (G.) peteri, S. (G.) takaokai), pH with two species (S. (S.) gravelyi and S. (S.) palmatum) and conductivity with two species (S. (G.) panagudiense and S. (G.) sp.) and S. (G.) kottoorense not related with these factors. For studying seasonal pattern of black fly distribution, Kulathupuzha River at ABR was selected for sampling. The physicochemical parameters of Kulathupuzha River for twelve months period are given in Table 6. A total of 7404 black fly larvae were collected under two subgenera Gomphostilbia and Simulium. Two species from Gomphostilbia (S. (G.) peteri and S. (G.) takaokai) and a species from Simulium (S. (S.) striatum) were identified. The larvae of Gomphostilbia were dominant (95%). S. (S.) striatum larvae were not considered for further analysis due to their petite distribution. Of 95% of Gomphostilbia immature, 40% of individuals account to leaf litter. Among the substratum, the leaf litter holds the higher number of larvae during sampling periods (Table 6). Black fly larvae were not found during May and June, due to dryness/summer. Overall, S. (G.) peteri was the dominant species, presenting density of 64% and they distributed in all stream substrates and, their maximum density was 36% in leaf litter followed by 26% in boulders, 14% in woody debris, 17% in bed rock and 6% in pebbles (Table 6). The highest percentage of S. (G.) peteri were observed in leaf litter during July (70%), in wood debris on December (24%), boulders and bed rock on April (43%, 25%) and in pebbles on December (14%). The larvae of S. (G.) takaokai showed a marked preference for leaf litter, with their distribution at higher number between December and February and
species, S. (S.) gravelyi (16%) and S. (S.) striatum (15.1%) were abundantly present. The most frequently distributed species was S. (S.) striatum (62.5%) followed by S. (G.) sp. (29.2%) and S. (S.) gurneyae (20.8%). Seven species: S. (S.) grisecens, S. (S.) palniense, S. (S.) palmatum, S. (S.) pattoni, S. (G.) takaokai, S. (G.) kottooresne and S. (G.) cauveryense were distributed between less than three streams. The highest diversity value was observed at site 19 (No. of taxa: 5; Shannon: 1.518; Simpson: 0.765) and eight sites (site number: 1, 3, 4, 8, 15, 16, 22, 23) had no diversity values, holding single taxa (Table 3). Among the distribution of black fly species in sampling sites of three regions, Five falls and Kallada River at ABR, Manjalaru and Moolayar at PWS and Kallar and Barliar at NBR had the highest similarity and other sites showed partial to low similarity revealed by the Jaccard’s similarity index. The same pattern was observed in the beta diversity indices (Table 4). Result of correlation coefficient analysis showed that the environmental variable of pH, stream order and latitude were interrelated with the distribution of taxa in streams than the other variables (Fig. 2). Further, for validating the above result, canonical correspondence analysis (CCA) was analyzed (Fig. 3). The eigen value and inter-site variability of CC-1 axis were 0.041 and 63.6% respectively. CCA result showed the latitude, stream order, pH and conductivity are significant variables for the distribution of black fly larvae. The result of Detrended correspondence analysis (DCA) was plotted in a scatter diagram (Fig. 4) and it shows the relationship between sites and species assemblages that sites 1 and 3 is closed with S. (G.) panagudiense followed by site 9 with S. (G.) takaokai, site 10 with S. (G.) peteri, site 4 with S. (G.) kottoorense, site 15 with S. (S.) gravelyi and site 16 with S. (S.) palniense. Based on the CCA result, the four environmental variables (pH, latitude, stream order and conductivity) were taken for further analysis to find the right factor responsible for species assemblage.
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Table 5 (continued)
Table 5 Statistical analysis between species (dependent) and environmental variables (independent) in 24 streams. Parenthesis-p value. Species
S. (S.) gravelyi
Statistical test
S. (S.) grisecens
S. (S.) lineothorax
S. (S.) striatum
S. (S.) gurneyae
S. (S.) palniense
S. (S.) pattoni
R2 F
0.08 0.72 (0.62)
t
0.96 (0.4)
S. (G.) peteri
S. (G.) takaokai
2
0.02 1.5 (0.23)
t
0.02 (0.9)
R2 F
0 1.8 (.16)
t
−0.24 (0.8)
R2 F
0 2.2 (0.1)
t
0.2 (0.8) 2
0.01 0.65 (0.6)
t
1.8 (0.01)
R2 F
0.15 1.7 (0.2)
t
1.11 (0.3)
R2 F
0.04 0.8 (0.5)
t
1.9 (0.1)
R F S. (S.) sp.
0.01 1.149 (0.37) 1.61 (0.1)
R F S. (S.) nilgiricum
2
t
R F S. (S.) palmatum
−0.14 (0.9)
t R F
Latitude
2
0.11 0.9 (0.4)
t
−1.71 (0.1)
R2 F
0.18 1.4 (0.2)
t
−1.51 (0.1)
R2 F
0.1 1.4 (0.3)
t
−0.86 (0.4)
R F
2
0.06 0.7 (0.5)
S. (G.) panagudiense
t
−2.26 (0.1)
R2 F
0.19 1.9 (0.9)
S. (G.) kottoorense
t
−0.99 (0.3)
R F S. (G.) cauveryense
2
3.34 (0.1)
t R F
0.06 0.6 (0.7)
2
0.19 3.76 (0.01)
pH
Stream order
Conductivity
0.79 (0.4) 0.03
−0.4 (0.7) 0
0.2 (0.9)
−0.41 (0.7) 0
0.55 (0.6) 0
0.1 (0.9)
1.22 (0.2) 0.08
2.1 (0.04) 0.13
−0.5 (0.6)
0.19 (0.9) 0
−0.1 (0.9) 0.04
−1.7 (0.1)
1.23 (0.2) 0.05
2.2 (0.04) 0.29
−0.8 (0.4)
−0.16 (0.8) 0
−1 (0.3) 0.01
−1 (0.4)
1.48 (0.2) 0.1
−0.8 (0.4) 0.06
−1 (0.3)
−1.26 (0.2) 0.07
−0.8 (0.4) 0.03
−0.8 (0.4)
−0.57 (0.5) 0
0.59 (0.6) 0
−0.1 (0.9)
0.58 (0.6) 0
0.99 (0.3) 0.04
−0.7 (0.5)
0.51 (0.6) 0.01
1.69 (0.1) 0.16
0.7 (0.5)
−0.36 (0.7) 0.01
1.2 (0.2) 0.11
−0.5 (0.6)
−0.84 (0.4) 0.04
0.07 (0.9) 0
1.9 (0.1)
−1.17 (0.3) 0.09
−0.3 (0.8) 0
−0 (0.9)
−2.7 (0.1) 0.12
2.12 (0.1) 0.07
−0.4 (0.7)
Species
Statistical test
Latitude
pH
Stream order
Conductivity
S. (G.) sp.
t
1.21 (0.2) 0.11 6.1 (0.001)
−0.8 (0.4) 0.04
4.7 (0.1)
R2 F
0.43 (0.7) 0.03
0.6
0 Bold-significant value.
0
July and August (Table 6). The highest percentage of association with stream substrates were: leaf litter on December (56%), woody debris on November and March (33%), bed rock on July (29%), boulders on November (31%) and pebbles on August (11%). Alpha diversity indices of Shannon and Simpson values were high (H: 1.49 ± 0.02, 1-D: 0.75 ± 0.06) between September and January. One-way ANOVA resulted that stream substrates were significantly (F = 5.502; P = 0.291) related with larval abundance. The effect of seasonality on two species distribution was analyzed individually by Correspondence Analysis (CA). In CA of S. (G.) peteri, eigen value of CA1 and CA2 axes were 0.043 and 0.029. Scatter plot based on CA axes score shows changes in black fly species among months (Fig. 5). CA result for S. (G.) peteri revealed that larval abundance was associated with leaf litter on July (Fig. 5). While, S. (G.) takaokai larval abundance was related to pebbles and boulders on October and their eigen value of CA1 and CA2 axes were 0.068 and 0.057.
0
0
0
0
0
4. Discussion The Oriental Region has the second largest black fly fauna than the other zoogeographical regions with 24% of the world total existing species. Of these, two subgenera Gompostilbia (37%) and Simulium (44%) consist of maximum number of species (Takaoka, 2017). Possibly, 16 species were collected under two subgenera Gomphostilbia and Simulium from 24 streams of three protected regions in South India. Among 16 species, 10 species were observed under the subgenus Simulium and rest of the species belongs to Gomphostilbia. Simulium (Simulium) striatum was common species and they distributed in more than 15 sampling streams and other species restrict to site specific or variation of environmental factors. Supportively, the distribution of black flies is influenced by the factors of breeding site characteristics, seasonal abundance, stream size and depth, food supply, substratum, velocity, light and physico-chemical conditions (Lake and Burger, 1983; McCreadie et al., 2006a; McCreadie et al., 2006b; McCreadie and Adler, 2012; Rabha et al., 2013). In this study, we observed that the three sampling sites (Moolayar and Silver cascade at PWS and Kunthipuzha at NBR) had the human discharges like sewage and solid wastes, whereas these sites hold many black fly larvae. However, other streams sites had less human impact and pristine streams with wide range of species distribution and black fly larvae were markedly different between sampling sites, as shown through beta diversity analysis. Hence, species richness was correlated with environmental variables by using CCA, suggesting that the four factors such as latitude, stream order, pH and conductivity were significantly related with larval assemblages. This outcome contradicts with the report of Figueiro et al. (2012) that leaf litter, rocky substrate, riparian vegetation and water velocity were significantly related with black fly assemblages and explained the
0
0
0.1
0
0
0.1
0
0
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Table 6 Physico-chemical parameters and abundance (%) of black fly larvae in five larval habitats of Kulathupuzha River (LL-Leaf litter, WD-Woody debris, BR-Bedrock, BO-Boulder, PE-Pebbles, n-total no. of larvae/12 months).
WAT (°C) STW (m) STD (cm) CUV (s cm−1) TDS (ppt) DSO (mg L−1) pH CON(μsec) SAL (ppm) CAC (5) SUI
Jan
Feb
Mar
Apr
May
Jun
Jul
Aug
Sep
Oct
Nov
Dec
26 5.8 21 0.06 184 9.2 7.2 286 21 50 7
25 5.4 20 0.07 195 9.1 7.3 296 22 50 7.1
27 4.9 19 0.1 210 8.9 7.5 302 25 50 7.3
28 4.1 18 0.2 190 8.2 7.2 278 20 45 7.4
0 0 0 0 0 0 0 0 0 0 0
29 3.1 12 0.05 185 8.8 7.2 212 23 50 7.9
27 4.3 15 0.05 170 9.1 7.2 235 24 50 7.3
25 5.2 20 0.05 160 9.5 7.2 254 24 50 7
25 5.8 20 0.02 180 10.3 7.3 241 25 50 7
23 6.1 25 0.01 190 9.6 7.3 256 25 50 7.5
21 7.5 26 0.01 160 9.8 7.4 278 22 50 7
20 7.1 25 0.05 175 10.1 7.3 281 22 50 6.9
S. (G.) peteri
LL WD BR BO PE n
38.8 10.3 12.9 31 6.9 7.3
37 10.9 18.1 29.7 4.35 8.7
40.8 12.7 14.8 31.7 0 8.9
16.7 15.3 25 43.1 0 4.5
0 0 0 0 0 0
0 0 0 0 0 0
70 0 16.7 6.67 6.67 1.9
34.6 21 17.3 25.9 1.23 5.1
33.3 18.5 15.6 19.3 13.3 8.5
27.5 17.3 20.7 26.4 8.14 18.6
30.4 17.8 16.8 24.8 10.2 19
27.7 24 10.3 24 14 17
S. (G.) takaokai
LL WD BR BO PE n
44.4 30.2 12.7 11.1 1.59 7.18
50 23.9 12.5 10.2 3.41 11
38.5 32.5 16 9.47 3.55 20
0 0 0 0 0 0
0 0 0 0 0 0
0 0 0 0 0 0
50 0 29.2 18.8 2.08 5.5
50.7 16.4 0 21.9 11 8.3
31.6 29.3 14.9 14.4 9.77 20
33.3 25.8 9.09 24.2 7.58 7.52
15.4 32.7 11.5 30.8 9.62 8.3
56 22 13.8 6.42 1.83 12.4
Note: WAT-water temperature, STW-stream width, STD-stream depth, CUV-current velocity, TDS-total dissolved solids, DSO-dissolved oxygen, CON-conductivity, SAL-salinity, CACcanopy cover, SUI-substrate index.
deeper (Pramual and Wongpakam, 2010). The seasonal pattern of the present study revealed that larval assemblages were peak in rainy seasons (South-west monsoon and North-east monsoon). The black fly larvae were highly associated with leaf litter than the other stream substrates. During south-west monsoon, the larvae of S. (G.) peteri were highly associated with leaf litter, whereas, S. (G.) takaokai association in north-east monsoon. The stream substrates of bedrock, boulders, stones and plant matter influence on the distribution of benthic fauna (Oliveira et al., 2014). Of these, plant material accumulated in streambeds promotes spatial heterogeneity, food and shelter for aquatic invertebrates (Carvalho and Uieda, 2010). This study illustrates the importance of spatio-temporal organization for determining the distribution of black fly in streams. Latitude, stream order, water pollution, water conductivity are the most important factors influencing species assemblages. The higher number of distribution was found in rainy season with leaf litter substratum. In particular, the present study highlights the spatial and temporal variations are the prime factor and act synergistic on the distribution of black flies as per the hierarchical structure obtained whereas as the anthropogenic impact is known to be a successive factor and works independently. Future research should be directed to conduct long-term data to track the response of black fly communities to environmental and climate change in streams.
competitive pressures in each microhabitat of sampling site determine the distribution of species. The CCA suggested the five significant factors were statistically tested to find the species specific relationship. Consequently, latitude and stream order related with eleven species, and conductivity and pH each with two species. The abundant black fly species of S. ochraceum and S. paynei, showed the spatial separation with substrates and altitudes and larval black fly distribution varied with environmental variables including stream size (Grillet and Barrera, 1997). In this study, latitude and stream order influence the population dynamics and community structure of many black fly species in South Indian streams, it supported by the following observations: physical characteristics of streams (McCreadie et al., 1995), physicochemical variables (McCreadie and Colbo, 1992), and biotic interactions (Hart, 1987). The close relationship between aquatic insect life cycle traits and spatial heterogeneity degree conferred ecological importance at the small scale level (Scarsbrook and Townsend, 1993) due to variability of stream substrates and heterogeneous environments (Resh et al., 1988). The improved precipitation would be enhanced dispersal of black fly larvae due to heavy water flow (Matthiessen et al., 2010). The marked differences were found in the distribution of black fly larvae between the dry and rainy seasons; however, species richness was significantly higher in the rainy season, when rivers are faster and
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Fig. 5. Correspondence Analysis representing the distribution of black fly larvae and seasonality in first and second axes in Kulathupuzha River of Southern Western Ghats.
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