Abstract

Biological invasions are a worldwide threat to the aquatic systems and have the potential to homogenize entire foodwebs and shift species abundance distributions to more skewed ones. Invasion impacts include effects on the foodweb structure and ecosystem functioning leading to a loss in native fish biodiversity and commercially important fisheries in many open water systems. The impacts of invasives are generally devastating as they spread in the foodweb with each species potentially interacting with multiple species. The foodweb modeling studies conducted in different inland aquatic ecosystems show that not all exotics cause a detrimental effect on the resilience of an ecosystem. Information on the foodweb structure and ecosystem properties is a prerequisite for formulating management protocols for conserving biodiversity, enhancement programmes and sustaining fisheries. The present paper reviews the impacts of invasive fishes in Indian aquatic ecosystems in the context of a changing foodweb scenario due to exotic fish species invasions. The information generated here could be applied for future research on similar ecosystems for deducing management actions.

Introduction

India has different climatic zones that support diverse aquatic habitats rich in aquatic biodiversity (Sarkar et al., 2017). In recent decades, the introduction of invasive fish is considered to be a major cause of species extinction posing a major ecological threat to the inland aquatic systems through the displacement of native fauna and alteration in the dynamics (Singh et al., 2014; David et al., 2017). The invasions will profoundly influence the function of the whole foodweb, and as a consequence the trophic relationships are impaired. In India, several studies have highlighted the occurrence of many invasive flora and fauna in inland ecosystems and also reported the consequences of the invasion at a regional scale (Paliwal and Bhandarkar, 2014; Singh et al., 2014; Sandilyan et al., 2018; Sarkar et al., 2017). Many studies have also shown that invasive species are a threat to endemic and threatened species in ecosystems throughout the world including important biological hotspots (Denslow, 2007; Raghavan et al., 2008). Biological invasion generally causes a decrease in the native biodiversity and population abundances (Kenis et al., 2009; Vilà etal., 2011; Singh et al., 2014), and affects the ecosystem functioning (Wardle et al., 2011; Simberloff et al., 2013). Romanuk et al., (2009) explored several foodwebs and invader properties that predispose a species to successfully invade and establish among the local communities. The alterations in an ecosystem arising from invasions usually lead to native species extinctions and a decline in local species richness.

Exotic fish have invaded inland aquatic systems in India from the aquarium traders and aquaculture farms (Krishnakumar et al., 2009; Singh and Lakra, 2011; Panikkar et al., 2015b). Many of the exotic fishes have established a good breeding population in inland systems and caused damage to the aquatic diversity (Singh and Lakra, 2011; Sandilyan, 2016). The impacts on ecosystems and biodiversity by invasives result in huge economic (Pimentel et al., 2000) and socio-cultural losses (Lockwood et al., 2007). The success of an invasion has a trade off with increased trophic interactions (Baiser et al., 2010). The number of connections the invader possesses influences its performance in the foodweb invasion. A few studies on this scale have been undertaken in the reservoir ecosystems over the last decade describing trophic structure and foodweb interactions for studying the impacts of invasions (Khan and Panikkar, 2009; Bijukumar et al., 2015; Gallardo et al., 2016). These studies have shown a linkage between foodweb interactions and invasion.

We conducted an investigation on the empirical studies of a few tropical reservoir ecosystems in India on how fish -invasions alter foodwebs in terms of ecosystem attributes and functions. The status of the impact of invasive fish on the aquatic ecosystems in India is synthesized and reviewed from the perspective of foodwebs. These studies provide information on the intensity of the impact of invasives and also address the knowledge gaps for management through an ecosystem approach.

Trophic interactions between invasive fishes and other fish groups in the foodweb

In India, few studies have been conducted to model the freshwater ecosystems using foodweb-based approach. These studies have reported the presence and impact of exotic fishes on the other fishes in the ecosystem. The geographical locations of these freshwater ecosystems in different states of India are illustrated in Fig. 1. Invasions have been found to profoundly influence the function of the whole foodweb and as a consequence the trophic interactions are impaired. Invasive fishes are considered to alter the foodweb of an ecosystem by reducing the food availability for the native fishes through competition for food thereby reducing the native populations and establishing themselves in the ecosystem. Impacts of invasives are generally devastating as they spread across the foodweb, as each species interacts with a number of different species. We expect negative consequences for the same reason. Khan and Panikkar (2009) developed a foodweb model (Fig. 2) of foodweb interactions in Kelavarapalli, a small reservoir in Tamil Nadu, India to quantify the energy flows between different trophic levels in the foodweb and to assess the impact of invasive fishes on other fishes in the foodweb.

Fig. 1

Map of India depicting the geographical locations of the reservoirs.

Fig. 1

Map of India depicting the geographical locations of the reservoirs.

Fig. 2

Diagrammatic representation of foodweb of Kelavarapalli reservoir ecosystem in India dominated by exotic fishes (Khan and Panikkar, 2009) P-Production; Q- consumption are the trophic flows in t km-1 year-1.

Fig. 2

Diagrammatic representation of foodweb of Kelavarapalli reservoir ecosystem in India dominated by exotic fishes (Khan and Panikkar, 2009) P-Production; Q- consumption are the trophic flows in t km-1 year-1.

The introduced Nile Tilapia, Oreochromis niloticus and the native Etroplus suratensis in the reservoir were found to have the highest prey-predator overlap (Fig. 3) that indicated a high competition for similar food resources. Indirect trophic effects through exploitation and competition also were found to affect the native groups but the invasives often have been considered to have positive bottom up effects on secondary consumers and apex predators in the foodweb. Predation is considered to cause the most remarkable damage in invaded aquatic systems, at times cascading down to the primary producers. Due to the complex prey-predator interactions, invasions have been found to greatly modify the structure of the entire foodweb.

Fig. 3

Prey-predator niche overlap plot in exotic fishes dominated in Kelavarapalli reservoir, India (Khan and Panikkar, 2009)[The ecological groups in box II have no overlap and are independent for both prey and predators. Groups in box III have a high overlap for both preys and predators. The numbers 2 to 10 represents different ecological groups as follows (2) Exotic African catfish (3) Indigenous catfishes (4) Snake head fishes (5) Exotic Mozambique Tilapia (6) Exotic Nile Tilapia (7) Pearl spots (8) Major carps (9) Dipterans (10) Zoo-benthos].

Fig. 3

Prey-predator niche overlap plot in exotic fishes dominated in Kelavarapalli reservoir, India (Khan and Panikkar, 2009)[The ecological groups in box II have no overlap and are independent for both prey and predators. Groups in box III have a high overlap for both preys and predators. The numbers 2 to 10 represents different ecological groups as follows (2) Exotic African catfish (3) Indigenous catfishes (4) Snake head fishes (5) Exotic Mozambique Tilapia (6) Exotic Nile Tilapia (7) Pearl spots (8) Major carps (9) Dipterans (10) Zoo-benthos].

The mixed trophic impact (MTI) studies which is a form of a sensitivity analysis in foodweb interactions, explain the influence of one ecological group on another (Majkowski, 1982). The MTI study in Kelavarapalli Reservoir, India indicated that an increase in the biomass of the highly invasive fish, the African walking catfish (Clarias gariepinus) would adversely affect almost all the fish groups in the reservoir. The Mozambique Tilapia (Oreochromis mossambicus) negatively impacted the indigenous catfishes whereas the Nile Tilapia (O. niloticus) was found not to adversely affect any one of the fish groups (Khan and Panikkar, 2009). A mass balance model for the Wyra reservoir in Telangana, India which has O. mossambicus in the fishery was developed (Panikkar and Khan, 2008). It is reported that the tilapia has a negative impact on a few fish groups such as the murrels, indigenous catfishes and barbs. Exotic carps, Cyprinus carpio and Grass Carp, Ctenopharyngodon idella were reported to have a negative impact on murrels and minor carps in Hemavathy reservoir in Karnataka (Khan et al., 2015). Oreochromis mossambicus in Vellayani Lake modeled by Bijukumar et al (2015) was found to have a strong adverse impact on barbs and carpels, and a slight impact on the other native fishes like the needle fishes, gobiids, and nandids. An increase in the biomass of Oreochromis sp. would have negative impact on many of the indigenous fishes, Puntius sp., Trichogaster fasciatus, Channa sp., Chanda ranga, Chanda nama, Batasio batasio in Bakreswar reservoir in West Bengal, India (Banerjee et al., 2016).

Effect of invasive fishes on the foodweb structure

Foodweb structure is an important constituent in understanding any ecosystem and ecologists around the world are investigating on this aspect (Christensen et al., 2005; Khan and Panikkar, 2009; Figueroa et al., 2009; Panikkar et al., 2015a,b; Murphy et al., 2019). The ecological summary indices for different foodwebs of the aquatic ecosystems studied in India are presented in the Table 1.

Table 1.

Ecological indicator for ecosystem health assessment of the inland aquatic systems modelled in India.

Inland ecosystemArea (ha)No. of Ecological groupsExotic fish in the systemTPP/TRTPP/TBTB/TSTCIOIFCIMPLAscen-dancyOver-headReference
Wyra reservoir, Telengana 1074 17 Oreochromis mossambicus, 1.367 16.24 0.011 0.246 0.191 NA 3.42 24.75 75.25 Panikkar and Khan, 2008 
Kelavarapalli reservoir, Tamil Nadu 430 14 Oreochromis niloticus,O. mossambicus,Clarias gariepinus 7.78 76.07 0.006 0.296 0.156 3.04 2.31 35.92 64.08 Khan and Panikkar, 2009  
Ravishankarsagar reservoir,Chattisgarh 9540 13 None 10.36 80.33 0.005 0.299 0.162 1.99 2.29 46.8 53.2 Panikkar et al., 2015a  
Hemavathy reservoir, Karnataka 9162 13 Cyprinus carpio, Ctenopharyngodon idella 5.33 72.58 0.005 0.264 0.112 NA 3.75 38.2 61.8 Khan et al., 2015  
Veli Lake, Kerala 30 14 None 7.5 12.26 0.012 NA NA NA NA NA NA Aravindan, 1993  
Vellayani Lake,Kerala 331.2 17 O. mossambicus 3.64 21.22 0.021 0.395 0.205 2.52 2.24 39.87 60.13 Bijukumar et al., 2015  
Bakreswar Reservoir, West Bengal 6740 27 Oreochromis sp. 1.72 9.73 0.05 0.176 0.109 8.44 3.08 25 75 Banerjee et al 2016 
Inland ecosystemArea (ha)No. of Ecological groupsExotic fish in the systemTPP/TRTPP/TBTB/TSTCIOIFCIMPLAscen-dancyOver-headReference
Wyra reservoir, Telengana 1074 17 Oreochromis mossambicus, 1.367 16.24 0.011 0.246 0.191 NA 3.42 24.75 75.25 Panikkar and Khan, 2008 
Kelavarapalli reservoir, Tamil Nadu 430 14 Oreochromis niloticus,O. mossambicus,Clarias gariepinus 7.78 76.07 0.006 0.296 0.156 3.04 2.31 35.92 64.08 Khan and Panikkar, 2009  
Ravishankarsagar reservoir,Chattisgarh 9540 13 None 10.36 80.33 0.005 0.299 0.162 1.99 2.29 46.8 53.2 Panikkar et al., 2015a  
Hemavathy reservoir, Karnataka 9162 13 Cyprinus carpio, Ctenopharyngodon idella 5.33 72.58 0.005 0.264 0.112 NA 3.75 38.2 61.8 Khan et al., 2015  
Veli Lake, Kerala 30 14 None 7.5 12.26 0.012 NA NA NA NA NA NA Aravindan, 1993  
Vellayani Lake,Kerala 331.2 17 O. mossambicus 3.64 21.22 0.021 0.395 0.205 2.52 2.24 39.87 60.13 Bijukumar et al., 2015  
Bakreswar Reservoir, West Bengal 6740 27 Oreochromis sp. 1.72 9.73 0.05 0.176 0.109 8.44 3.08 25 75 Banerjee et al 2016 

(Abb: TPP- Total Primary production, TR- Total Respiration, TB- Total Biomass, TST -Total System Throughput, CI-Connectance Index, OI- Omnivory index, FCI-Finns cycling Index, MPL-Mean Path Length, NA -Not available)

The introduction of fish in a system through stock supplementation can cause substantial effects on the foodweb (Mbabazi et al., 2004). A mass-balanced model study in Hemavathy, a large reservoir in Karnataka, southern state of India was conducted for two periods (before and after the introduction of fish seeds) using ECOPATH to assess the impact of non-native fish seed stocking on the foodweb of the ecosystem (Khan et al., 2015). In this particular reservoir, non-native carps Cyprinus carpio and the grass carp, Ctenopharyngodon idella were stocked along with the Indian major carps (Catla catla, Labeo rohita and Cirrhinus mrigala). The biomass of the non—native carp group was estimated as 0.447 and 2.56 t km-1 year-1 in the fishery during 1982-83 (pre-stock phase) and 2002-03 (post-stock phase) respectively (Khan et al., 2015). The mixed trophic impact routine showed that an increase in biomass of the non-native carps showed a slight negative impact on the eels but did not impact any other fish groups in the ecosystem.

In the Hemavathy reservoir of Karnataka, India (Khan et al., 2015), the trophic flows basically happened in the first four trophic levels and the food -web was characterized by the predominance of low trophic level organisms during the two different phases which were modelled. The comparative trophic models showed a variation in the foodweb structure and system summary statistics in the reservoir during the two phases despite the changes in biomass of the natives and non-native fishes (Khan et al 2015). Connectance index (CI) and omnivory index (OI) are ecological indicators that are correlated with the maturity of the reservoir ecosystem as described by Odum (1971). The OI and CI values showed a decline after the non-native fish seed stocking in Hemavathy reservoir and the difference in these values indicate that the post-stock phase of the ecosystem displayed less web-like features which is a positive impact of fingerling stocking. The Vellayani lake in Kerala which has an invasive population of O. mossambicus modeled by Bijukumar et al (2015) had the highest OI for the newly introduced Indian major carps (0.38) indicating that they exploit the niches available in the ecosystem winning the competition with other fishes.

Impact of invasive fish on the ‘health’ of an ecosystem

The health of an ecosystem has been measured using Odum’s attributes of system maturity (Christensen, 1995). The Ecopath model provides various tools which help in developing various attributes that can be used in assessing the state of health of an ecosystem. A healthy ecosystem is not easily vulnerable to disturbances, both anthropogenic and natural. A comparative analysis of different time periods for the same system can help managers to assess the health status of the system (Christian et al., 1996). The network analysis which indicate the health status consisting of algorithms that describe the system attributes through foodweb dynamics (Christensen, 1998). These are effective tools in assessing the impacts of exotic species induced perturbation on ecosystems (Miehls, 2009). A comparative statement of the ecosystem health indicators for the different inland ecosystems modeled in India are presented in Table.1. This section gives an account of various ecological indicators that helps in assessing the health of an ecosystem.

As described in the previous section CI and OI are also indicators of ecosystem maturity and these values tend to increase as the ecosystem matures (Odum, 1971). The system’s OI of Vellayani lake was 0.205 suggesting a low omnivory in the system. The CI was 0.395 indicating a high diversity of trophic compartments that can be expected in tropical lakes with rich biodiversity. These indicators point to the immaturity of the lake.

The informational indices also called the flow indices, such as, the ascendency and overhead have also been shown to be related to maturity of an ecosystem (Christensen, 1995). The highest overhead values were obtained for Wyra followed by Kelavarapalli reservoir ecosystems which has a composition of exotics in the fishery (Table 1).

Finn’s cycling index, as described by Finn (1976), is the fraction of the recycled throughput of an ecosystem and is an indicator of the system’s resilience and stability (Odum, 1969). The high value of FCI represents a mature and healthy ecosystem and low values are typical of vulnerable ecosystems that are sensitive to nutrient input alterations as reported by Christensen and Pauly (1993). FCI of Vellayani lake was 2.52 % of the total system throughput of the system and the MPL was 2.24 which further indicates the developing stage of the lake. Ravishankarsagar reservoir with an FCI of 1.99 is indicative of a developing ecosystem. FCI of Bakreswar reservoir system was relatively very high (8.44%) showing least vulnerability compared to the other ecosystems.

The flow of energy through a foodweb is expressed by Finn (1976) in terms of Mean Path Length (MPL) which is the number of trophic interactions of each ecological group. The addition of fish into the system did not affect the stability of the system as in the case of Hemavathy reservoir which showed an increase in MPL by 14%. (Khan et al., 2015). The system was found to be more stable after systematic fish stocking (which included non- native carps) in the reservoir.

We conducted a study on the fish species composition and catch structure of Manchanbele reservoir in Karnataka, India and developed the foodweb model. This reservoir was dominated by exotic fish (O. niloticus) in the late 1990. Due to structured stocking with Indian major carps (IMC) there was a shift in fishery from the dominance of exotic fishes to IMCs (ICAR-CIFRI, 2016). The exotics to IMC ratio in 2010-11 was 4:3 which gradually changed to 1:3 in 2017-18. The foodweb model of Manchanbele reservoir showed a CI value of 0.31 that is comparable with the values of Ravishankarsagar reservoir (Panikkar et al., 2015a) as depicted in Table 1. This shows that the presence of exotics may not adversely affect the resilience of the ecosystem.

In Wyra Reservoir, Panikkar and Khan (2008) observed that the system as a whole presents mean transfer efficiencies very analogous in the two phases (a very small difference of 0.1% the total system’s carrying capacity) which shows that the general foodweb structure remains similar despite the changes of abundance of the various indigenous fish groups such as murrels, cichlids, catfishes, gobids, major carps, barbs, minnows and prawns) including the invasives (tilapia) in the system.

Foodweb approach for managing exotic fish invasions

Management of exotic species invasion in inland waters is a challenge worldwide and hence needs considerable attention. The impacts of an invasive fish could refer to positive or negative environmental and socio-political alterations that these species can cause in the systems (Shackleton, 2007;Binimelis et al., 2008; Kull et al., 2011, Gallardo et al., 2016). Based on the situation, exotic species can cause alterations in the ecosystem properties of the invaded systems or on human livelihood (Blackburn et al., 2014; Bacher et al., 2018; Shackleton et al., 2019). The range and intensity of these intrusions make management of inland aquatic ecosystems a challenging task and these challenges can be tackled through ecosystem management approach (Christensen et al., 1996; Khan and Panikkar, 2009).

Globally, there are several guidelines and management protocols formulated to deal with the invasive species (Piria et al., 2017). In India, presently, there are no proper management policy to address the issues associated with the introduction and establishment of exotic species in inland aquatic systems. The United Nations’ Sustainable Development Goals for 2030 highlights the need for protecting aquatic life and invasive species management (Ives et al., 2019). To meet the objective of ecosystem approach of management and to assess the impact of exotic species invasion in inland systems on the foodweb, it is imperative to understand the trophic function of the ecological change that is happening within the system (Khan and Panikkar, 2009). Ecosystem models play a vital role in the ecosystem approach to management of aquatic systems and they provide inputs in identifying the properties and potential changes in complex ecosystems that cannot be identified with single-species models (Christensen and Pauly, 1998).

Ecosystem modeling using the Ecopath with Ecosim (EwE) approach has been largely used as a tool to assess the ecosystem properties, explore the trophic interactions, fisheries monitoring and management (Christensen et al., 2005; Heymans et al., 2016). The present review on ecopath modeling studies conducted in the freshwater ecosystems of India to illustrate the intensity of the impacts also address the knowledge gaps and suggest recommendations for better management and prevention of exotic invasion in the country. The information derived from this method aids in developing conservation and management guidelines to mitigate the effects of the invasion. The EwE is being attempted to provide information on how ecosystems are likely to respond to changes in fishery management practices and therefore, suggested as a tool for designing ecosystem approach to fisheries (Plaganyi, 2007). The need to understand and quantify ecosystem behaviour and conditions has come to the forefront of environmental planning and policy formulations, particularly in view of the contemporary paradigm of ecosystem-based fishery management (Bijukumar et al., 2015).

Adequate information on foodweb structure and ecosystem function provide vital information on the effects of invasives on the ecosystem and provide a baseline for management of aquatic resources (Winemiller and Polis, 1996; Ives et al.,2019). Such information has relevance for developing management strategies aimed at managing exotic invasive fishes and conserving the biodiversity (Khan and Panikkar, 2009; Ives et al., 2019).

Conclusions

The inland open waters in India are vulnerable to exotic fish invasion and there is a need to develop a national level database on invasive fish in different aquatic systems. To effectively manage the invasive in a system, there has to be some general rules on regional basis as to which management responses are efficient to deal with invasion events. This involves steps taken to (i) prevent invasive species from entering a new habitat (ii) if introduced, efforts to remove if they become well established (iii) actions to limit negative impacts and to retain any benefits of the species if they become widely established (Shackleton et al., 2017; Novoa et al., 2019).

We found that many empirical studies on bio-invasions have focused on the species specific aspects while a few have adopted the foodweb perspective. Species-specific approaches run a risk of bias and tend to ignore the interaction between different causes of invasion at the ecosystem level. The foodweb approach is one of the most intuitive conceptualizations of an ecosystem. The information presented and discussed here forms a basis for future research planning on changing foodweb interactions with the introduction of exotics in the aquatic system.

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