Abstract

Meenachil River originates from the biodiversity hotspot Western Ghats, home to varied and diverse fish fauna endemic to the region. The fish composition of the upper, middle and lower stretches of the Meenachil River was investigated from 2015 to 2019 to explore the fish assemblage patterns and the associated environmental factors. Thirty-nine species belonging to 20 families, 11 orders, and 31 genera were collected during the study. Order Cypriniformes ranked first with 16 species, followed by Siluriformes and Anabantiformes, each with five species. Three major assemblage patterns were differentiated in Meenachil River, the “mountainous species,” inhabiting the upstream, “piedmont species,” the midstream; and the “downstream species,” the lower stretches. Canonical Correspondence Analysis reflected altitude as the most significant factor influencing the assemblage pattern of fishes in the Meenachil River. Nemacheilus triangularis, Garra mullya, Barilius gatensis, Barilius bakeri and Haludaria fasciata, with a strong negative correlation to salinity, TDS, and conductivity, supported their partitioning and distribution restricted only to the high altitude areas of the river. Piedmont species positively correlated to dissolved oxygen levels were Mystus montanus, Rasbora daniconius, Devario aequipinnatus, Mastacembelus armatus and Salmostoma acinaces. Glossogobius giuris, Systomus sarana, Hyporamphus limbatus, Mystus gulio, Mystus oculatus, Etroplus suratensis, Parambassis dayi and Gerres setifer showed very strong positive correlations to salinity, TDS and conductivity were restricted to the downstream. Megalops cyprinoides is an anadromous species migrating between Vembanadu Lake and the lower stretches of the river. Etroplus maculatus, Parambassis thomassi, Aplocheilus lineatus, Dawkinsia filamentosa, and Xenentedon cancila have general distribution in the river not significantly influenced by any of the environmental parameters studied. Deviations from the existing structural pattern in fish assemblages can be used to assess the ecological status of the river and its fish fauna.

1. Introduction

The major challenge in the conservation ecology of riverine ecosystems is understanding the structure and functioning of their community composition ¹. Fish assemblages are among the most valid indicators of the ecological condition of streams and rivers ². Understanding the natural variation of fish assemblages is crucial for developing and implementing stream management plans ³. As fishes occupy at or near the peak of the food chain, they can serve as indicators of balanced aquatic ecosystems ^{4, 5}. The geomorphologic attributes, as well as the biotic and abiotic environmental variables, are the major forces that structure the fish communities of a river both in terms of species richness and distribution of individual species ^{6, 7, 8}. Effective management of a riverine system requires reliable information about its water quality parameters ⁹. One of the important threats faced by the riverine fish fauna is the severe water quality deterioration where they dwell. The decline in biodiversity is far more significant in freshwaters than in the most affected terrestrial ecosystem ¹⁰. Presently, the anthropogenic influences on the aquatic systems go far beyond the natural variations, leading to a drastic reduction in water volume and the quality of water in Indian rivers ¹¹. The riverine systems are particularly vulnerable because they lack the volume of open marine waters, limiting their capacity to dilute the contaminants ¹².

Freshwater Ichthyology studies in Kerala can be traced back to the late 18th century with the work of Bloch ¹³, followed by Jerdon ¹⁴ and Day ¹⁵. After the works of Francis Day, studies of freshwater fishes in Travancore were resumed through the significant contributions from Hora ¹⁶, Menon ¹⁷, Devi et al. ¹⁸, Easa and Shaji ¹⁹, Raghavan et al. ²⁰ and Kumar ²¹. Although many studies have been conducted on Kerala's riverine fish diversity, only a few works have been done on the fish assemblage patterns of rivers. Studies were conducted on the estuarine fish fauna of Kodungallur and Vembanadu Lake of Kerala ^{22, 23} and the fish assemblage attribute for the streams and rivers of other southern states of India sharing the Western Ghats ²⁴. The present study attempts to assess the water quality parameters and their influence on the fish assemblage attributes of the Meenachil River of Southern Western Ghats, Kerala, India.

2. Material and Methods

Meenachil River originating from the Western Ghats is a perennial river 78kms long with a basin area of 1272 km². The river confluence to India’s second largest wetland ecosystem, Vembanad Lake, before getting emptied into the Arabian Sea. The watershed of the river extends from a latitude of 9^o25’ to 9^o55’ and a longitude of 76^o20’ to 76^o55’ ²⁵.

Seven representative sampling sites were selected along the river's entire stretch falling in upstream, midstream, and downstream areas from the headwaters to the mouth, the Vembanad Lake (Figure 1). Sampling location details are given in Table 1. Sites were selected based on the accessibility and physical features of the habitats (Figure 2, Figure 3, Figure 4)

The study period spans five years, from January 2015 to December 2019. Based on the southwest monsoon, which significantly influences the climate in Kerala, the seasons were categorized into pre-monsoon, monsoon, and post-monsoon, respectively. Sampling was conducted during the different seasons with the help of fishing experts and local fishermen.

Traditional and unique fishing methods developed by the local fishing community were also adopted to collect specific species (Figure 5, Figure 6, Figure 7). Least number of fishes was collected from the river for identification and the rest were immediately released into the river without harming. Identifications were done referring the standard literature ^{21, 53, 57}. Conservation status of fishes was documented according to the IUCN criteria.

SAMPLING SITES

SAMPLING METHODS

Water quality parameters were evaluated in-situ at each sampling site using a Multi-parameter portable meter, HANNA, Model HI 2020-02, which included water temperature (ATC, °C), conductivity (COND, µSm/cm), total dissolved solids (TDS, mg/L), dissolved oxygen (DO, mg/L), salinity (ppt) and pH. Water samples were collected from various sampling sites from Meenachil River during the pre-monsoon, monsoon, and post-monsoon seasons and were periodically analyzed from 2015 to 2019. The altitude of the sampling sites was provided by GPS, which also provided the value for basic coordinates, latitudes, and longitudes (Table 1).

Spider graphs display data using multivariate discrete dimensions spaced equally around the circle. All axes radiate out from a centre point of origin, representing a single dimension ranging from zero to maximum value. In the present study, spider graphs were used to represent the variation in hydrological parameters over the different seasons from 2015 to 2019 (Figure 9 - Figure 14). Each variable was plotted along its individual axis, and the entire data over five years from different geographical zones of the river was represented in two dimensions.

Canonical Correspondence Analysis (CCA) ²⁶ was performed to find out the relationship between different species of the fish assemblage and how they are influenced by environmental variables. This is an ordination technique designed for the direct analysis of relationships between multivariate ecological data ²⁷. The statistical significance of CCA relationships between the set of environmental factors and fish species of the river was evaluated using a Monte Carlo permutation test with 999 permutations. The statistical analysis was done using the software PAST ²⁸. CCA of a site/species matrix has generated values for the environmental variables assessed during the study (Figure 15). The ordination axes are linear combinations of environmental variables. CCA is a method of direct gradient analysis where the gradient in environmental variables is a known prior, and the species abundance is considered to be a response to this gradient. The implementation follows Eigen analysis algorithms given in ²⁶. The ordinations are given as site scores, and the environmental variables are plotted as correlations with site scores. The length of a vector for a given environmental variable indicates the importance of that variable in the analysis. The biplot of the species and site score produced from CCA shows the distribution of species and the sites in ordination space.

3. Results

A total of thirty-nine species belonging to 20 families, 11 orders, and 31 genera were collected during the study, which included two vulnerable (VU) species, five data deficient (DD), two nearly evaluated (NE), and 30 least concerned (LC) species (Table 3). Order Cypriniformes ranked first with 15 species followed by Siluriformes and Anabantiformes, each with five species (Figure 8). Out of the 39 species reported, 18 were endemic to the Western Ghats (WG), and one endemic to the Kerala region (KL). Two exotic species (EX) were also reported during the study. Devario aequipinnatus, Garra mullya, Dawkinsia filamentosa are widely distributed in India and are common and abundant species in Western Ghats Rivers. Their vast distribution and abundance reflected their tolerance to fluctuating environmental factors ⁵³.

A maximum water temperature 31.1°C was recorded at midstream station Mutholy during the pre-monsoon of 2015 and a minimum of 25°C at Theekoy headwaters during the monsoon of 2017 and 2019. No significant difference was found in temperature among the different sites during different seasons (Figure 13). pH values fluctuated between a minimum of 5.21 at Poonjar station during the pre-monsoon of 2017 and a maximum of 7.40 at Cherpunkal during the post-monsoon of 2018 (Figure 12). Total dissolved solids (TDS) showed significant variations between the different sites during different seasons from 2015 to 2019. A maximum value of 365ppm was recorded at downstream site Kumarakom during the monsoon of 2015 and a minimum of 11.03ppm at the upstream zone Bharananganam during the post-monsoon of 2018. Mean TDS ranging from 17.929 ppm to 172 ppm reflected the variation between the sites during different seasons (Figure 10). Conductivity showed significant variations between the stations during different seasons from 2015 to 2019. A maximum conductivity of 815µSm/cm was noticed at Kumarakom during the pre-monsoon of 2015 and a minimum of 21.67µSm/cm at Theekoy during the post-monsoon of 2017. The mean conductivity ranging from 42.71 to 353.07µSm/cm reflected significant variation between the upper and lower stretches of the river (Figure 9). Kumarakom station at the confluence zone reported a maximum salinity of 0.4ppt during the post-monsoon of 2019. The average salinity value ranged from a minimum of 0.07 to 0.4ppt (Figure 11). A minimum dissolved oxygen concentration of 2.64mg/L was recorded at Kumarakom during the pre-monsoon of 2015 to a maximum of 7.69mg/L at upstream station Teekoy during the monsoon of 2018. The mean range varied from 6.12mg/L to 4.42mg/L. Dissolved oxygen content showed significant variations between stations during different seasons from 2015 to 2019 (Figure 14).

Three major assemblage patterns (Figure 15) could be differentiated based on the distribution of fish species along the CCA axis. The first assemblage, Quadrant 1, was negatively correlated to CCA2 and positively correlated to CCA1, denoting they occupied the mountainous area of the upstream geographical zone at high altitudes. Altitude shows the highest eigengard value, 0.4525, with the longest vector representation having the most significant influence on fish species distribution in the Meenachil River (Table 2).

Five species in Quadrant 1 inhabiting the upstream tributaries, Theekoy, Poonjar, and Bharanaghanam, were grouped together and defined as “mountainous species,” they were Nemacheilus triangularis, Garra mullya, Haludaria fasciata, Barilius bakeri, Barilius ghatensis. The remaining species in quadrant one laid close to the CCA1 axis, and those in quadrant two were grouped as “piedmont species.” These include the transitory species Salmostoma acinaces, Salmostoma bacalia, Hypselobarbus kurali lying close to the CCA 1 axis, which transits from the mountain to the piedmont sites of midstream. The remaining piedmont species include Anabas testudineus, Puntius punctata, Mystus montanus, D. aequipinnatus, Puntius mahecola, Rarsbora daniconius, Wallago attu, Piaractus brachypomus. and Mastacembelus armatus. Piedmont species and those species that transit between piedmont sites and downstream were negatively correlated to pH. Species S. acinaces and R. daniconius inhabited sites with relatively high levels of dissolved oxygen and low levels of TDS and conductivity and were highly influenced by these factors.

Species positively correlated to CCA 2 and negatively correlated to CCA1 in quadrant three were divided into two groups. Groups 1, those strongly influenced by salinity were Gerris setifer and S. sarana found only in low altitudes. The remaining species closely associated with the CCA2 axis were transitory between the midstream and lower stretches of the river, forming Group 2. These species include L. dussumieri, O. mossambicus, P. mahecola, C. diplogramma, C. marulius, H. fossilis, E. fluviatilis, W. attu and P. brachypomus. Species negatively correlated to CCA1 and CCA2 in quadrant four, along with the transitory species Megalops cyprinoides is the low land species inhabiting the downstream confluence zone of the river with high TDS and conductivity and low levels of dissolved oxygen. The species inhabiting low altitude site Kumarakom are Hyporhamphus limbatus, Mystus gulio, Mystus oculatus, Etroplus suratensis, Glossogobius giuris, Parambassis dayi, and G. setifer.

Species distributed around the center of the CCA biplot have a more general distribution throughout the entire stretch of the river, being insignificantly influenced by any of the environmental parameters. Those species included Etroplus maculatus, Parambassis thomassi, Applocheilus lineatus, D. filamentosa, and Xenentodon cancila which had a common distribution in the river.

4. Discussion

Physico-chemical parameters play a significant role in determining the species richness and abundance in a relatively small spatial scale or single drainage system ^{7, 44} as in Meenachil River. Canonical Correspondence Analysis revealed three distinct fish assemblages from the headwaters to the mouth of the Meenachil River. Fish assemblage pattern along the longitudinal gradient of a river reflects homogenous spatial units within the riverine system ^{29, 30}. The partitioning of fish assemblages can be well explained by multiple factors acting along the longitudinal gradient of the river, which include the availability of resources, water quality parameters, quality of habitats, and the ability of individual species to adapt ³¹.

The headwater “mountainous species” were highly specialized to adapt to the frequent flow disturbances in their habitat. Mountainous species are endemic and restricted to the upstream tributaries at high altitudes within specific habitats, riffles, pools, rapids, and cascades having pebble substratum with strong water currents. The fish assemblage of an upstream geographical zone has unique morphological adaptations to survive even in extreme flow variations ^{32, 29}. G. mullya, endemic to the upstream zones, was highly structurally adapted to seasonal flow alterations and water volume variations. Suctorial adhesion created by the highly specialized adhesion disc of G. mullya forms a cavity with a vacuum by the contraction of its muscles helps to overcome the drastic flow alterations during the high monsoon showers and destructive landslides ^{33, 34}. CCA analysis clearly reflected altitude as the most significant factor influencing the mountainous species, N. triangularis, G. mullya, H. fasciatus, B.bakeri and B. gatensis as seen in Quadrant 1 of the CCA biplot (Figure 15). These altitude-influenced fishes showed a positive correlation with dissolved oxygen levels, and a strong negative correlation with salinity, TDS, and conductivity supporting their partitioning and distribution restricted only to the high altitude zone of the river, including the sites, Poonjar, Theekoy, and Bharanangaanam, with the lowest levels recorded for conductivity, TDS and salinity (Figure 9, Figure 10, Figure 11). DO is positively correlated with altitude, which has a significant influence on the distribution of the upstream species (Figure 14). Reference ³⁵ mentioned the significance of dissolved oxygen as one of the most influencing factors in fish distribution and abundance upstream.

The open channel, side channels, or tributaries linked to flood plains and varying substrate types favor both fluvial specialists and habitat generalist fish species of “piedmont” ³⁶. The piedmont species of the Meenachil River were significantly influenced by the regular monsoons and associated flooding. The leaf litter and organic debris from the riparian promote the lateral exchange of nutrients during the annual floods, which could have a positive influence on the piedmont fish fauna ^{37, 38}.

The difference in feeding habits, choice of food resources, and habitats results in a more complex assemblage in the midstream of rivers ³⁹, which was noticed in the heterogeneity of piedmont species of the midstream stretch of Meenachil River, including L. dussumieri, O. mossambicus, P. mahecola, C. diplogramma, C. marulius, H. fossilis, E. fluviatilis, W. attu and P. brachypomus with varied feeding preferences. The inhabitants in tributaries linked to the flood plain wetlands of Meenachil River were C. striata, C. marulius, H. fossilis, A. testudineus, which were omnivorous ^{40, 52}; W. attu, piscivorous ⁴¹; and M. armatus with insectivorous feeding habits ⁴². The most abundant species of midstream, L. dussumieri preferred algae, which proliferates during the south-west monsoon.

The migration of low-land fishes upstream occurs for reproduction ^{30, 43}. The spawning migration supports the species addition factor, which brings a shift in species composition ⁴⁵. The massive breeding migration of L. dussumieri reported from the lower stretches to upstream, occurring annually in the Meenachil River, supports the findings of ⁴⁵. Check dams along the river usually prevent the fish migration of transitory species ²⁹. The low-land species were found to be transitory migrants from the estuarine zone to the upstream stretches for reproduction. H. kurali is another downstream species of Meenachil River found migrating from lower stretches to upstream for breeding.

Among the hydrobiological attributes, salinity, TDS, and conductivity have been identified as the crucial determinants of fish assemblage in the downstream estuarine stretch of rivers ^{46, 47}. The fishes in quadrants 3 & 4, G. giuris and S. sarana; H. limbatus, M. gulio, M. oculatus, E. suratensis, P. dayi, and G. setifer showed very strong positive correlations to salinity, TDS, and conductivity. M. cyprinoides was the transitory species of this assemblage that migrates between the Vembanadu Lake and lower stretches of the Meenachil River. The assemblage of estuarine species at Kumarakom was negatively correlated to altitude and dissolved oxygen and was restricted to the downstream confluence zone of the Meenachil River.

The decline of water quality in the downstream zone was reflected in the higher values for TDS, 365ppm (Figure 10) and conductivity, 815µSm/cm (Figure 9), and the least value for dissolved oxygen, 2.64mg/L (Figure 14) reported in the Kumarakom site during the post-monsoon of 2019. Some of the water quality variables should be considered in terms of point and non-point pollution sources over small scales ^{48, 4}. The nitrates and nitrites produced due to the breakdown of accumulated organic wastes in the stagnant waters could have resulted in eutrophication and algal blooms. Mass mortality of fish was reported due to algal blooms and depletion of dissolved oxygen levels during the pre-monsoon season from the confluence zone of the Meenachil River ⁴⁹.

Reference ⁴⁹ reported the significant impacts of the changes in habitat variables on the fish distribution pattern of major rivers of Kerala. Sources for TDS included agricultural runoff, urban runoff, and industrial waste, natural resources such as decomposing leaves, silt, and weathering rocks. Conductivity and TDS downstream of the Meenachil River were found to increase from December to May and decrease from June to November (Figure 9, Figure 10). This was due to the shutting down of the Thanneermukkom bund, the barrage constructed across Vembanadu Lake to prevent saltwater intrusion from the Arabian Sea to the associated agricultural fields. This has caused a temporary stagnation during the pre-monsoon period in the lower stretches of the river as well as in the Lake where the river confluences ⁵⁴, supporting the higher values recorded for Conductivity, TDS, and the varying salinity in the Kumarakom downstream site of the Meenachil River (Figure 9, Figure 10, Figure 11).

Abrupt transitions could be observed when the physio-chemical conditions become stressful, and only a fewer fish species are able to survive ^{30, 50}, which could result in species replacement or additions. Opportunistic migration of less tolerant species from highly polluted downstream to the midstream zone was also noticed in the present study, which could have resulted in deviations from the expected patterns of the fish assemblage of the Meenachil River. The transition of E. fluviatilis and E. suratensis from the downstream confluence zone to the midstream stretches and the replacement of native species downstream by more adaptable transitory ones like M. cyprinoides noticed in the present study was in accordance with the above finding.

A perusal of the literature revealed that the Pacific Tarpon M. cyprinoides are highly adapted fishes with a modified air bladder that enables them to inhale atmospheric oxygen and tolerate oxygen deficiency ⁵¹, enabling them to live in highly polluted environments. The abundance of this particular species was noticed as an indicator of heavy stream pollution ⁵⁵, which could be attributed to the declined diversity and deteriorated water quality in the downstream stretch of the Meenachil River. The lowest dissolved Oxygen levels, variations in salinity, and total dissolved solids reported in 2019 from the downstream of Meenachil River (Figure 10, Figure 11) were in line with the findings of ⁵⁵. Reference ⁵⁶ reported the ability of M. cyprinoides to tolerate a wide range of salinities.

5. Conclusion

Three major assemblage patterns were differentiated in Meenachil River based on the distribution of fish species along the CCA axis- “mountainous species,” inhabiting the upstream tributaries, “piedmont species,” inhabiting the midstream, including the transitory species between the upstream and midstream, and the “downstream species” which also included the transitory species between the midstream and downstream. CCA analysis reflected altitude as the most significant factor influencing the assemblage pattern of the river. The mountainous species showed a strong negative correlation, restricting their distribution only to the high-altitude areas of the river. In contrast, the downstream species showed a strong positive correlation to TDS, conductivity, and salinity distributed exclusively to the lower stretches. The piedmont and transitory species are moderately influenced by the different environmental parameters, dissolved oxygen, and salinity. E. maculatus, P. thomassi, A. lineatus, D. filamentosa, X. cancila, having a common distribution in the river, was not significantly influenced by any of the environmental parameters studied. M. cyprinoides is the transitory species of this assemblage that migrated between Vembanadu Lake and the lower stretches of the river. TDS and conductivity downstream increased from December to May and decreased from June to November due to the closure of the Thanneermukkom barrage constructed across the Lake and Arabian Sea.

An in-depth understanding of the pattern of organization of fish community composition of the river helps document the fish status by exploring the mechanisms responsible for the changes in fish diversity patterns to develop effective stream management plans. Species restricted to a particular zone of the river act as significant indicators of ecological integrity. Deviations from the existing structural pattern in community composition can be used in the future to assess the ecological status of the river and its fish fauna. The present study reflected the significant fluctuations in water quality parameters TDS, conductivity, salinity, and dissolved oxygen levels, especially in the downstream zone, which reflected anthropogenic influences and pollution in the tourism-dominated lower stretches of Meenachil River. Legal measures should be taken to minimize pollution in the lower stretches of the Meenachil River, promoting sustainable tourism development with biodiversity conservation perspectives.

Acknowledgements

The authors are grateful to the Principals, Dr. Varughese Mathew, Dr. Icy K John, and Research Coordinator Dr. Neetha Nair, of Mar Thoma College Tiruvalla, for providing the necessary work facilities. We are greatly indebted to the fishing craft and gear operators Mr. Thankakuttan, Mr. Jony, Mr. Saji, and the “Meenachil River Restoration Forum” officials Mr. Philip Mani and Mr. Abdulla Khan for their support during the fieldwork and data collection.

Conflict of interest

The authors declare that they have no conflicts of interest.

References