Table of Contents Author Guidelines Submit a Manuscript
International Journal of Zoology

Volume 2014, Article ID 191059, 8 pages

http://dx.doi.org/10.1155/2014/191059
Research Article

Life Cycle and Secondary Production of Four Species from Functional Feeding Groups in a Tropical Stream of South India

1Department of Environmental Biotechnology, Bharathidasan University, Tiruchirappalli 620 024, India

2Department of Zoology, The Madura College, Madurai 625011, India

Received 4 June 2014; Revised 31 July 2014; Accepted 3 August 2014; Published 20 August 2014

Academic Editor: Thomas Iliffe

Copyright © 2014 Sankarappan Anbalagan et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

This study focused on life strategies of species from functional feeding groups (FFGs) found in a tropical stream of the Sirumalai hills, South India. We examined the life cycle and secondary production of species of shredders (Lepidostoma nuburagangai), scrapers (Baetis sp.), collectors (Choroterpes alagarensis), and predators (Neoperla biseriata). In addition, we studied the assemblage structure of functional feeding groups. We found the collectors occupied the highest percentage, followed in turn by scrapers, predators, and shredders. The diversity of FFGs was higher at riffle areas and assemblage with stream substrates differing in each functional group. An asynchronous life cycle was observed for Baetis, C. alagarensis, and N. biseriata, while L. nuburagangai was found in four to five generations per year. We acquired data on secondary production of scraper species of Baetis, which reached the highest values among all investigated species. This observation stresses the importance of scrapers as playing a key role in converting coarse particulate organic matter to fine particulate organic matter with low or high abundances of shredder population and maintaining the food chain in tropical streams.

1. Introduction

Tropical forests cover 15–20% of the earth’s land surface and about half of this is being converted to agricultural land and for other human purposes. More than 50% of the world’s biodiversity is found in the tropical forests. Freshwater ecosystems are relatively more important than the terrestrial ecosystems because aquatic organisms are highly susceptible to climatic variation and anthropogenic impact [1]. The allochthonous organic substrate provides protection and habitat space and it has fundamental importance as a food source for aquatic macroinvertebrates [2]. Aquatic macroinvertebrates are classified into four major functional feeding groups (FFGs) based on the morphobehavioural mechanisms of food acquisition rather than taxonomic groups as follows: shredders, scrapers, collectors, and predators [3].

Feeding measures that contribute to fluvial trophic dynamics encompass FFGs and provide information on the balance of feeding strategies (food acquisition and morphology) in the benthic assemblage [4]. The major food sources utilized by macroinvertebrates are the epilithic layer that grows on the surfaces of substrates (consumed by scrapers), the coarse detritus of leaves falling from riparian vegetation (consumed by shredders), the fine detritus either deposited on the substrate or suspended in the water column (consumed by collector/filter-feeders), and live animals (consumed by predators) [35].

The knowledge of FFGs has been widely studied throughout the world and is central to the River Continuum Concept [6]. FFGs are also used in water quality assessment [4, 7], energy transfer studies [8, 9], and food chain modelling [10], but information is lacking on the life cycle and secondary production of FFGs in tropical regions, especially India. The threats faced due to tourism, grazing, hunting, poaching, agriculture, deforestation, and land use have resulted in a loss of aquatic biodiversity in India [1113]. Therefore conservation of existing and functionally important species is an urgent need to preserve the aquatic biodiversity in India. In this study, we examined the life cycle pattern and secondary production of aquatic insect species from the four major functional feeding groups. In addition, we studied the assemblage structure of functional feeding groups in a tropical stream of South India.

2. Materials and Methods

2.1. Study Area

The present study was carried out in a tropical stream (Thadaganachiamman stream) of South India between June 2007 and May 2008. The Thadaganachiamman stream of the Sirumalai hills is in the Eastern half of the Dindigul District. The Sirumalai hills form a minor range in the Deccan plain (latitude: 10°, 08′, 12′′N, longitude: 78°, 01′, 08′′E, and elevation: 375 m) of the Western Ghats and is a hilly region whose elevation ranges from 250 to 800 m.a.s.l. This perennial stream is situated about 32 km from Madurai city (Figure 1). The rainfall is between 156 and 195 cm ann−1, unevenly distributed through the year with the highest rainfall received during the north-east monsoon (November) and south-west monsoon (June–August). Along the banks of the stream are thick stands of trees and shrubs whose leaves are the stream’s principal source of organic detritus. Dominant riparian tree species are Pongamia pinnata (common name: Pongam or Indian Beech tree), Syzygium cuminii (Jamun), and Commiphora caudata (Hill Mango). The prominent herbs on the banks of the stream are Cyperus bulbosus, Cyperus dubius, Fimbristlis schoenoides, Cyanotis cristata, and Commelina clavata.

191059.fig.001
Figure 1: Study area—Siurmalai hills, southern India.
2.2. Sampling Methods

Month-wise sampling was done at study site of Thadaganachiamman stream. The physicochemical parameters and a stream profile were measured by Dinakaran and Anbalagan [14] and APHA [15]. In the study area, three 50 × 50 cm benthic samples were taken at random locations from riffle and pool. The sampling depth of riffle and pool of the stream ranged from 10 to 15 cm and 50–80 cm, respectively. Samples were collected in riffles, using 180 μm mesh kick-nets and 500 μm mesh dip nets used for pool sampling. Adult insects were sampled by sweep netting in the vegetation of stream corridor to confirm species identifications and determine emergence periods. A light trap was also used to collect adults. Soon after collection, the specimens were preserved in 70% ethanol.

2.3. Laboratory Analysis

All collected specimens were identified and classified based on their feeding pattern and morphological characters according to Dudgeon [5]. Further, the gut of specimens from each functional taxon was dissected out and the presence of taxa in the gut was observed under a stereoscopic dissection microscope to confirm the trophic category of four major functional feeding groups. The body length and head width of the four functional taxa were measured using an ocular micrometer in a stereoscopic dissecting microscope. Body lengths were converted to body mass for secondary-productivity calculations using dry mass length equations given in Benke et al. [16]. Individuals from all sites were combined to provide a large enough sample for production analysis. Further, secondary productivity was calculated using the size frequency method for all species and the instantaneous growth rate method for species where cohorts could be reliably separated [17].

2.4. Data Analysis

The distributional difference of aquatic insects between riffle and pool was estimated by one-way ANOVA. Size-frequency histograms based on body length and head width of four functional taxa were plotted using the software package, PAST version 2.08, and graphs were edited with Photoshop software. To test the relationship between body length and head width of taxa, linear regression was used. In this analysis, data was log transformed and estimated by the generalized linear regression model. The relationship of population density, biomass, and production of the four species was tested with two nonparametric tests of Kruskall-Wallis and Friedman test by using the software package, PAST version 2.08.

3. Results

The physicochemical parameters of the study area are given in Table 1. In total, 19 species belonging to 15 families and 8 orders of aquatic insects were collected from both riffle and pool areas of the stream. The collected specimens were classified based on their feeding pattern into shredders, scrapers, collectors, and predators. Among functional feeding groups of this stream, the collectors occupied the highest percentage (52%), followed by scrapers (18%), predators (16%), and shredders (14%). FFGs diversity was significantly (, ) related to riffle than the pool area revealed by one-way ANOVA. The shredders and scrapers were primarily associated with leaf litter at pool, while collectors and predators were predominant in riffles where they were found in the substrates of bedrock, boulders, pebbles, leaf litter, and woody debris (Table 2). The monsoonal effects altered the distribution of aquatic insects, with the high diversity and abundance found during postmonsoonal period (,   ).

tab1
Table 1: The physicochemical parameters (mean ± SE) of a Thadaganachiamman stream in the Sirumalai hills of Southern India.
tab2
Table 2: Density (individuals/m2) of functional feeding groups in the stream substrates.

Dominant species were selected from each functional feeding group of shredder, scraper, collector, and predator for studying life cycle pattern and secondary production. Lepidostoma nuburagangai Dinakaran et al. [18] as a shredder, Baetis sp. as a scraper, Choroterpes alagarensis Dinakaran et al. [19] as a collector, and N. biseriata Zwick et al. [20] as a predator were taken for this study. The gut analysis of these four functional species was done to confirm the respective trophic category. The fragments of leaf and wood in the gut of L. nuburagangai, large amounts of diatoms, periphytons, and plant detritus in the gut of Baetis, periphytons, diatoms, and fine detritus in the gut of C. alagarensis and animal materials in the gut of N. biseriata were observed (Table 3).

tab3
Table 3: The gut contents of functional feeding groups (mean ± SE).

Size frequency histograms for body length and head capsule width of L. nuburagangai revealed four separate cohorts: the first cohort hatched from eggs in June, with rapid growth followed by adult emergence in August; a second cohort hatched from eggs in September and grew for 4 months and adults emerged in December; the third cohort hatched from eggs in January and grew for 1-2 months and adults emerged in February; the fourth cohort hatched from eggs in March and grew for 1-2 months and adults emerged in April and May (Figure 2). The cohorts of Baetis and C. alagarensis showed asynchronous nymph development with continuous emergence except during the summer (Figures 3 and 4). N. biseriata showed four generations that could be easily separated throughout the autumn, winter, spring, and summer, but the major emergence took place in early summer (March and April), with the new generation appearing in the samples in July. Adults of N. biseriata were found between May and August and December and January (Figure 5).

fig2
Figure 2: Size frequency distribution of L. nuburagangai, (a) body length (mm), and (b) head width (mm) (HA—hatching; EM—emergence).
fig3
Figure 3: Size frequency distribution of (a) body length (mm) and (b) head width (mm) of Baetis sp.
fig4
Figure 4: Size frequency distribution of (a) body length (mm) and (b) head width (mm) of C. alagarensis.
fig5
Figure 5: Size frequency distribution of (a) body length (mm) and (b) head width (mm) of N. biseriata.

Linear regression equations indicated that the body length and head width of all four species were significantly correlated (Figure 6). The population density, biomass, and production of the four functional taxa were significantly related as shown by one-way ANOVA, Friedman test and Kruskal-Wallis test. The total annual secondary production of Baetis reached the highest values (514 mg m−2 y−1) among all investigated species. The high production of these taxa was observed during July, January, and April, which reflects higher densities occurring in these months, whereas lower production was observed between October and December. The ratio of productivity to biomass (P/B ratio) indicated four to five cohort productions in L. nuburagangai and eight to nine cohort productions in Baetis sp. and C. alagarensis sp. and N. biseriata (Table 4).

tab4
Table 4: Secondary production estimates (mean ± SE) for the four functional taxa using the size frequency method.
fig6
Figure 6: Linear regression model for head width and body length of four functional taxa.

4. Discussion

According to the River Continuum Concept [6], middle order streams were dominated by collectors, scrapers, predators, and shredders. Similarly, third order stream of the present study area had the highest percentage of collectors. This may be due to the enormous FPOM concentration available in the study sites. The highest aquatic insect diversity was observed in riffle areas due to the rich variety of substrates available in this habitat that provides habitat heterogeneity for the colonization of aquatic insects in streams. Similar results were found in other streams of South India [11]. In this study the highest diversity and abundance of aquatic insects were observed during postmonsoonal periods. The low insect abundance and diversity during monsoon are probably due to heavy water flow or flood. Leaf litter in the pool had its highest abundance of shredder and scraper species. The high insect abundance in pools during postmonsoon and low insect abundance in depositional areas (pools) during the dry season (March) are likely due to the fluctuation of physical and chemical parameters [21, 22]. Habitat heterogeneity is an important factor influencing macroinvertebrates distribution in streams [23]. Similar results were found in the streams of India [24].

Most permanent streams in the temperate zone have both autumn-winter and spring-summer growth periods while shredder species had two generations per year [25]. L. nuburagangai had four to five generations per year. In temperate forest streams, leaf fall occurs mainly in the autumn [26], whereas, in tropical streams, year-round leaf litter input [27], which may favour the additional generations for shredders. This finding contrasts with the study of Yule et al. [28], they reported the lack of insect shredder hosts and other shredding consumers, including fishes, shrimps, crabs, and prosobranch snails in tropical streams. The shredder L. nuburagangai occupies a key role in the energy and nutrient transfer from terrestrial to stream ecosystems. However, the fact that all life stages of L. nuburagangai are present at any given time maximizes exploitation of the continuous allochthonous input in tropical streams and facilitates population turnover. The P/B ratio of L. nuburagangai cohort was 4.8 or 5 a ratio indicating higher growth rates [29]. Bright [30] who reviewed the present knowledge of secondary production in inland waters concluded that yearly P/B ratios depend primarily on voltinism. Yule et al. [28] has pointed out that the dependence of the benthos on allochthonous material results from the highest biomass occurring in winter and early spring in temperate streams. This appears also to be true for the shredder of L. nuburagangai as their biomass was high during early spring (April-May).

Baetis species have been found elsewhere to be abundant in macrophytes and roots of marginal vegetation in riffles and pools [31]. Likewise, the South Indian Baetis was abundant in macrophytes and ubiquitous in pools and riffles. Baetis is associated with macrophytes because they support periphytic algae, which is food for the nymphs. The importance of autochthonous foods for macroinvertebrate production in forest streams was unexpected, but this has been reported elsewhere. Fujitani [32] showed that benthic algae were an important component in the diet of mayfly larvae in a Japanese stream. Baetis exhibited asynchronous development with most size classes present throughout the year in these South Indian streams. The same pattern was observed in tropical streams of Hong Kong [33] with similar annual production, but lower than the Australian stream [34], while higher than a Neotropical Costa Rica stream [35].

Size frequency diagrams and P/B ratio revealed that C. alagarensis had asynchronous development with year-round emergence. Water temperature could be one factor affecting this pattern, because it also influenced the growth of C. alagarensis during winter and summer. The thermal equilibrium hypothesis [36, 37] predicts that each species has an optimum temperature that allows maximum reproductive success and population stability.

N. biseriata was multivoltine and their major emergence was in early summer. A similar life cycle pattern has been reported in tropical streams of northern Florida [38] and an Appalachian stream in Pennsylvania [39]. Hilsenhoff et al. [40] reported that stoneflies were very common in a Wisconsin stream, with an emergence period from early April to early May. Giberson and Garnett [41] recorded emergence in May in a stream in northern New Brunswick. N. biseriata nymphs in this study stream have shorter life cycles and higher survivorship and reach their terminal nymphal biomass more rapidly than N. clymene [38] suggesting the factors involved are higher stream temperatures and/or nutrient concentration in study stream.

This result reflects the fact that leaf litter in a tropical stream serves as food for macroinvertebrates [2] and predicts the production of functional feeding groups especially shredders [3]. This study found evidence that fallen leaves from streamside vegetation enter the stream in all months, while a substantial portion of leaf input occurs during January and June and thus supported high densities of FFGs in Kallar stream of southern India [42]. Similarly, the fast growth of shredders during January and June and asynchronous development of other FFGs (scrapers, collectors, and predators) occurred throughout the year in the present study. Among the four investigated species of FFGs, the secondary production of scraper species (Baetis) had the highest values (514 mg m−2 y−1), which indicates that scraper plays a key role in converting allochthonous organic matter to fine particulate organic matter when low or high abundances of shredders occurs, thus maintaining the food chain in this tropical stream.

Conflict of Interests

The authors declare that there is no conflict of interests regarding the publication of this paper.

References

  1. O. E. Sala, F. S. Chapin III, J. J. Armesto et al., “Global biodiversity scenarios for the year 2100,” Science, vol. 287, no. 5459, pp. 1770–1774, 2000. View at Publisher · View at Google Scholar · View at Scopus
  2. E. F. Benfield, “Comparison of litterfall input to streams,” Journal of the North American Benthological Society, vol. 16, no. 1, pp. 104–108, 1997. View at Publisher · View at Google Scholar · View at Scopus
  3. R. W. Merritt, K. W. Cummins, M. B. Berg et al., “Development and application of a macroinvertebrate functional-group approach in the bioassessment of remnant river oxbows in southwest Florida,” Journal of the North American Benthological Society, vol. 21, no. 2, pp. 290–310, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. R. E. Uwadiae, “Macroinvertebrates functional feeding groups as indices of biological assessment in a tropical aquatic ecosystem: implications for ecosystem functions,” New York Science Journal, vol. 3, no. 8, pp. 6–15, 2010. View at Google Scholar
  5. D. Dudgeon, Tropical Asian Streams: Zoobenthos, Ecology and Conservation, Hong Kong University Press, Pokfulam Road, Hong Kong, 1999.
  6. R. L. Vannote, G. W. Minshall, K. W. Cummins, J. R. Sedell, and C. E. Cushing, “The river continuum concept,” Canadian Journal of Fisheries and Aquatic Sciences, vol. 37, no. 1, pp. 130–137, 1980. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Bij de Vaate and T. I. Pavluk, “Practicability of the Index of Trophic Completeness for running waters,” Hydrobiologia, vol. 519, no. 1–3, pp. 49–60, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Tomanova, E. Goitia, and J. Helešic, “Trophic levels and functional feeding groups of macroinvertebrates in neotropical streams,” Hydrobiologia, vol. 556, no. 1, pp. 251–264, 2006. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Blanchet, G. Loot, and J. J. Dodson, “Competition, predation and flow rate as mediators of direct and indirect effects in a stream food chain,” Oecologia, vol. 157, no. 1, pp. 93–104, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. V. V. Gertseva, J. E. Schindler, V. I. Gertsev, N. Y. Ponomarev, and W. R. English, “A simulation model of the dynamics of aquatic macroinvertebrate communities,” Ecological Modelling, vol. 176, no. 1-2, pp. 173–186, 2004. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Dinakaran and S. Anbalagan, “Habitat aptness and spatial heterogeneity of aquatic insects in Western Ghats: linking multivariate analysis,” The Ecoscan, vol. 2, no. 1, pp. 51–60, 2008. View at Google Scholar
  12. S. Anbalagan, J. Pandiarajan, S. Dinakaran, and M. Krishnan, “Effect of tourism on the distribution of larval blackflies (Diptera: Simulium) in Palni hills of South India,” Acta Hydrobiologica Sinica, vol. 35, no. 4, pp. 688–692, 2011. View at Google Scholar
  13. S. Anbalagan, S. Dinakaran, and M. Krishnan, “Spatio-temporal dynamics of leaf litter associated macroinvertebrates in streams of peninsular India,” Ecologia, vol. 2, no. 1, pp. 1–11, 2012. View at Google Scholar
  14. S. Dinakaran and S. Anbalagan, “Anthropogenic impacts on aquatic insects in six streams of south Western Ghats,” Journal of Insect Science, vol. 7, article 37, 2007. View at Google Scholar · View at Scopus
  15. APHA, Standard Methods for the Examination of Water and Wastewater, American Public Health Association, Washington, DC, USA, 16th edition, 1995.
  16. A. C. Benke, A. D. Huryn, L. A. Smock, and J. B. Wallace, “Length-mass relationships for freshwater macroinvertebrates in North America with particular reference to the southeastern United States,” Journal of the North American Benthological Society, vol. 18, no. 3, pp. 308–343, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. A. C. Benke, “Secondary production of aquatic insects,” in The Ecology of Aquatic Insects, V. H. Resh and D. M. Rosenberg, Eds., pp. 289–322, Praeger Publishers, New York, NY, USA, 1984. View at Google Scholar
  18. S. Dinakaran, S. Anbalagan, and C. Balachandran, “A new species of Caddisfly (Trichoptera: Lepidostomatidae: Lepidostoma) from Tamil Nadu, India,” Journal of Threatened Taxa, vol. 5, no. 1, pp. 3531–3535, 2013. View at Google Scholar
  19. S. Dinakaran, C. Balachadran, and S. Anbalagan, “A new species of Choroterpes (Ephemeroptera: Leptophlebiidae) from a tropical stream of south India,” Zootaxa, no. 2064, pp. 21–26, 2009. View at Google Scholar · View at Scopus
  20. P. Zwick, S. Anbalagan, and S. Dinakaran, “Neoperla biseriata sp. n., a new stonefly from Tamil Nadu, India (Plecoptera: Perlidae),” Aquatic Insects, vol. 29, no. 4, pp. 241–245, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. L. G. Oliveira, Aspects da biologia de communidades de insetos aquaticos da ordem Trichoptera Kirby, 1813, em corregos de cerrado do municipio de Pirenopolis, Estado de Goias [Tese de Doutorado], Universidade de Sao Paulo, Sao Paulo, Brazil, 1996.
  22. R. M. Kikuchi and V. S. Uieda, “Composicao da comunidae de invertebrados de um ambiente lotico tropical e sua variacao especial e temporal,” in Ecologia de Insetos Aquaticos, J. L. Nessimian and A. L. Carvalho, Eds., vol. 5 of Series Oecologia Brasiliensis, pp. 157–174, PPGE-UFRJ, Rio de Janeiro, Brazil, 1998. View at Google Scholar
  23. M. R. Vinson and C. P. Hawkins, “Biodiversity of stream insects: variation at local, basin, and regional scales,” Annual Review of Entomology, vol. 43, pp. 271–293, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Anbalagan and S. Dinakaran, “Seasonal variation of diversity and habitat preferences of aquatic insects along the longitudinal gradient of the Gadana River Basin, South-West Ghats (India),” Acta Zoologica Bulgarica, vol. 58, no. 2, pp. 253–264, 2006. View at Google Scholar
  25. N. H. Anderson and E. Grafius, “Utilization and processing of allochthonous material by stream Trichoptera,” Verhandlungen der Internationalen Vereinigung für Theoretische und Angewandte Limnologie, vol. 19, pp. 3083–3088, 1975. View at Google Scholar
  26. J. R. Webster and E. F. Benfield, “Vascular plant breakdown in freshwater ecosystems.,” Annual review of ecology and systematics. Vol. 17, pp. 567–594, 1986. View at Google Scholar · View at Scopus
  27. L. J. Benson and R. G. Pearson, “Litter inputs to a tropical Australian rainforest stream,” Australian Journal of Ecology, vol. 18, no. 4, pp. 377–383, 1993. View at Google Scholar · View at Scopus
  28. C. M. Yule, M. Y. Leong, K. C. Liew et al., “Shredders in Malaysia: abundance and richness are higher in cool upland tropical streams,” Journal of the North American Benthological Society, vol. 28, no. 2, pp. 404–415, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. A. D. Huryn and J. B. Wallace, “Life history and production of stream insects,” Annual Review of Entomology, vol. 45, pp. 83–110, 2000. View at Publisher · View at Google Scholar · View at Scopus
  30. G. R. Bright, “Secondary benthic production in tropical Island stream,” Limnology and Oceanography, vol. 27, no. 3, pp. 472–480, 1982. View at Google Scholar
  31. R. A. Jenkins, K. R. Wade, and E. Pugh, “Macroinvertebrate-habitat relationships in the River Teifi catchment and the significance to conservation.,” Freshwater Biology, vol. 14, no. 1, pp. 23–42, 1984. View at Publisher · View at Google Scholar · View at Scopus
  32. T. Fujitani, “Species composition and distribution patterns of baetid nymphs (Baetidae: Ephemeroptera) in a Japanese stream,” Hydrobiologia, vol. 485, pp. 111–121, 2002. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Salas and D. Dudgeon, “Life histories, production dynamics and resource utilisation of mayflies (Ephemeroptera) in two tropical Asian forest streams,” Freshwater Biology, vol. 48, no. 3, pp. 485–499, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. R. Marchant, “Estimates of annual production for some aquatic insects from the La Trobe River, Victoria.,” Australian Journal of Marine & Freshwater Research, vol. 37, no. 2, pp. 113–120, 1986. View at Publisher · View at Google Scholar · View at Scopus
  35. A. Ramírez and C. M. Pringle, “Structure and production of a benthic insect assemblage in a neotropical stream,” Journal of the North American Benthological Society, vol. 17, no. 4, pp. 443–463, 1998. View at Publisher · View at Google Scholar · View at Scopus
  36. B. W. Sweeney and R. L. Vannote, “Size variation and the distribution of hemimetabolous aquatic insects: two thermal equilibrium hypotheses,” Science, vol. 200, no. 4340, pp. 444–446, 1978. View at Publisher · View at Google Scholar · View at Scopus
  37. R. L. Vannote and B. W. Sweeney, “Geographic analysis of thermal equilibriums, conceptual model for evaluating the effect of natural and modified thermal regimes on aquatic insect communities,” The American Nature, vol. 115, pp. 667–695, 1980. View at Google Scholar · View at Scopus
  38. A. K. Rasmussen, Species diversity and ecology of Trichoptera (Caddisflies) and Plecoptera (Stoneflies) in Ravine ecosystems of Northern Florida [Ph.D. thesis], University of Florida, 2004.
  39. S. A. Grubbs and K. W. Cummins, “Linkages between riparian forest composition and shredder voltinism,” Archiv für Hydrobiologie, vol. 137, no. 1, pp. 39–58, 1996. View at Google Scholar · View at Scopus
  40. W. L. Hilsenhoff, J. L. Longridge, R. P. Narf, K. J. Tennessen, and C. P. Walton, Aquatic Insects of the Pine-Popple River, Wisconsin, Technical Bulletin no. 54, Wisconsin Department of Natural Resources, Madison, Wis, USA, 1972.
  41. D. J. Giberson and H. L. Garnett, “Species composition, distribution, and summer emergence phenology of stoneflies (Insecta: Plecoptera) from Catamaran Brook, New Brunswick,” Canadian Journal of Zoology, vol. 74, no. 7, pp. 1260–1267, 1996. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Anbalagan, T. Pratheep, S. Dinakaran, and M. Krishnan, “Effects of two leaf litter species on the colonization of macroinvertebrates in a tropical stream of India,” The Bioscan, vol. 7, no. 3, pp. 533–538, 2012. View at Google Scholar