Freshwater gastropod richness patterns along an urbanization gradient in tropical India

Abstract

Data on the urbanization impact on freshwater biota and ecosystem function are limited from many developing countries despite being recognized as a driver for biodiversity loss. To study these impacts, we analysed the species richness and diversity patterns of freshwater gastropods along a gradient of urbanization in a river system around Pune city, India. We observed a significant reduction in species richness, faunal similarity and an increased proportion of non-native species with increasing urbanization. These impacts were prominent in highly urbanized sites of the rivers suggesting biotic homogenization. Our results underscore the great impacts of urbanization on freshwater biota, highlighting the need for further studies in developing regions.

Introduction

Urban areas are continually expanding, especially in developing regions, driven by population growth (McKinney 2006; Aida et al. 2016; McKinney et al. 2018). India has many highly urbanized zones that are spreading rapidly and severely impacting biodiversity (Nagendra et al. 2013). Globally, increasing urban development causes increased pollution, environmental modifications and significant changes in land-use patterns (Elmqvist et al. 2016; Guetté et al. 2017). Such disturbances affect biodiversity and regional ecology, often leading to species extinctions and ‘Biotic Homogenization (BH)’—high biotic similarity between habitats at various scales (Rahel 2002). BH is fuelled by several factors including environmental changes, pollution, habitat alteration and species invasions, all of which typically result from urbanization (McKinney 2006).

Freshwater ecosystems are highly stressed largely due to anthropogenic disturbances, particularly urbanization (Dudgeon et al. 2006; Smith 2016). Urbanization alters hydrological processes like sediment deposition, water-holding capacity of river basins, amount and content of the organic matter and nutrient concentrations (Zope et al. 2017) often causing eutrophication (Smith 2016; Dodds and Smith 2016). Aquatic ecosystems in India are especially vulnerable to these threats, as ‘development and restoration’ projects often ignore detailed ecological assessments. Impacts of urbanization on many aquatic organisms, especially invertebrates, are well documented globally (Rahel 2002; Liu et al. 2020), but reliable data from India are still lacking.

Freshwater gastropod molluscs are common and important components of freshwater habitats ranging from rivers to small ditches and comprise highly endemic and globally invasive species (Strong et al. 2008). Their sensitivity to stressors, ecological specialization and their central role in ecosystem function makes them important indicators of biotic and abiotic changes in aquatic ecosystems (Bódis et al. 2016).

We examined the influence of urbanization on the distribution of freshwater gastropods in a river system running through the city of Pune in tropical India. We specifically assessed the relationship of species richness and β-diversity with increasing urbanization. We expect that an increase in urbanization would (1) reduce species richness, (2) increase the proportion of non-native species and (3) reduce the faunal similarity between high- and low-urbanized sites.

Materials and methods

Pune is one of the fastest growing cities in India (Krishnamurthy et al. 2016). We sampled seven different sites on four tributaries (Indrayani, Pawana, Mula and Mutha) (Fig. 1; Supplementary Fig. S1 and Supplementary Table S1) of the River Bhima, one of the major rivers in peninsular India. All these rivers traverse through the highly urbanized Pune Metropolitan Region. Qualitative sampling was carried out on a 100-m transect at each site, from the banks and the littoral zone by (1) visual surveys of aquatic vegetation and substratum, (2) handpicking and (3) a 250-μm hand net. The benthic regions could not be sampled due to a lack of specialized equipment. Snails were identified following Subba Rao (1989) and Ramakrishna and Dey (2007) and a species incidence (presence/absence) dataset was generated.

We used Domisch et al. (2015) 1-km resolution Near-global freshwater-specific environmental variables for biodiversity analysis dataset to extract the average urban/built-up (%) data for the sampling sites. We generated 150 random points around each site to obtain unbiased representative estimates (in this case, the average). A bounding box (0.01° latitude and longitude) was created around each site (‘bbox’ function) and the random points were generated within the box (‘spsample’ function) using the ‘raster’ package (Hijmans et al. 2015). Sites were then broadly categorized as sites with low urban built-up (mean urban built-up 2–17%; Sites 1–4) and with high built-up (mean urban built up >25%; Sites 5–7). The geographical distance between sites was calculated using DiVA-GIS (v7.5).

We used linear regression modelling to assess (1) the changes in the species richness and faunal similarity as a function of urbanization (represented as mean percent urban built-up and pairwise difference in mean percent urban built-up, respectively) and (2) spatial patterns in community similarity using inter-site distance and faunal similarity. The faunal similarity between the sampling sites was assessed using the Jaccard’s index on the species incidence data. Pairwise Jaccard’s values were also used to generate network plots with successive cut-off thresholds to visualize the β-diversity patterns relative to urbanization. Analyses were performed in PAST (Hammer et al. 2001) and RStudio (v.1.3.9).

Results

A total of 13 species were observed in the collection (Supplementary Table S2; Supplementary Fig. S2 for images of a few species). Species richness of freshwater gastropods declined sharply and significantly with increasing urban built-up (R² adj. = 0.75, F = 19.22, P = 0.007; Fig. 2A), from 9 to 12 (Sites 1–4) to 2 to 3 (Sites 5–7). Non-native species [Amerianna carinata (H. Adams, 1861), Physella acuta (Draparnaud, 1805)] comprised a higher proportion of total fauna (33–50%) in highly urbanized Sites (5–7) relative to the other sites (Fig. 2A).

The faunal similarity decreased significantly with increasing difference in percent urban built-up between sampling sites (R² adj. = 0.59, F = 40.43, P < 0.001; Fig. 2B). Sites with low urban built-up had a higher faunal similarity relative to difference in percent urban built-up when compared with those with high urban built-up. Faunal similarity increased between sites with high urban built-up areas in different rivers, whereas it decreased slightly for sites with low urban built-up (Fig. 2B).

A network analysis of the β-diversity patterns (Fig. 3) showed that the high urban built-up sites had low faunal similarity (<30%) to the sites with low urban built-up (indicated by the low weight of the edges connecting them) (Fig. 3A, B). Successively increasing cut-off thresholds separated the two groups corresponding to the degree of urbanization, where high (>70%) faunal similarity was observed among low urban built-up sites relative to that among high urban built-up sites (Fig. 3C–E).

Significant distance decay of faunal similarity between sampling sites (R² adj. = 0.64, F = 50.22, P < 0.001; Fig. 3F) was observed (see Fig. 3F and Supplementary Table S3 for pairwise similarity values). Faunal similarity increased with inter-site distance in highly urbanized sites (in different rivers) but decreased in the low urban built-up sites (Fig. 3F). Similar trends were observed in sites in the same river with highly urbanized site pairs showing reduced similarity, while low-urbanized sites showing a higher similarity among upstream and downstream fauna (see Figs 1 and 2; Supplementary Table S3).

Discussion

Urbanization drastically modifies the physicochemical aspects of freshwater habitats by altering their structure, hydrology and nutrient concentrations thereby affecting their biota, including molluscan fauna (McKinney 2006; Molur et al. 2011, Tolley-Jordan et al. 2015). Urban development in watersheds decreased the gastropod species richness in our study (Figs 1 and 2). However, the effects of these impacts depend on the faunal group studied, e.g. odonate richness increased with urbanization (Kulkarni and Subramanian 2013), while native fish species richness decreased with a subsequent increase in the non-native fish species (Dahanukar et al. 2012) in Pune region.

We observed only two to three gastropod species at the sites with high urban built-up (Supplementary Tables S1 and S2). These sites also showed low pairwise similarity despite being on the same river. The loss of habitat heterogeneity, commonly observed in urban environments due to increasing disturbance events, can lead to such a pattern. The flow channels at Sites 5–7 were altered and discharge of untreated sewage and garbage was rampant (AB personal observation). Higher chemical oxygen demand and lower dissolved oxygen (DO) values indicated increased organic pollution near Sites 5–7 relative to Sites 1–4 (Supplementary Table S1). Organic pollution and higher NO₃ concentrations have a negative effect, while high DO content positively influences the species richness in freshwater gastropods (Bódis et al. 2016), indicating the habitat unsuitability of some of the sampling sites in our study. The differences in the local environment may also have influenced the β-diversity patterns, wherein the less urbanized sites were taxonomically rich and shared many native species as opposed to highly urbanized habitats which were taxonomically poor and shared only non-native species (Supplementary Table S2).

Species invasion in aquatic ecosystems has been strongly linked to increased anthropogenic impact that can alter communities by eliminating native fauna and promoting the establishment of non-native species, which can rapidly extend their range (Bódis et al. 2016; Petsch 2016). This was observed with the increasing proportion of non-natives in highly urbanized sites, relative to the ones with low urban growth. The invasive P.acuta, first reported from Mula river almost 25 years ago (Subba Rao et al. 1994), but presently found in all four rivers (Supplementary Table S2) highlights this speed, which could profoundly alter the fauna in Indrayani and Pawana. Non-native species, especially aquatic ones, are often linked to the aquarium pet-trade and pose a serious concern for ecosystems globally. Unfortunately, due to the lack of baseline data in many Indian ecosystems (Molur et al. 2011), making a true assessment of the impacts of anthropogenic activities and introduced species is challenging.

This reduction in diversity and increasing proportion of non-native species (observed at the highly urbanized sites) are characteristics of BH, where biotas become increasingly similar reflecting an increased homogeneity in environments (Rahel 2002; Petsch 2016). This increased faunal similarity was observed specifically in rivers in highly urbanized areas contrasting the patterns in rivers in areas with low urban built-up (see Figs 2 and 3F). Although preliminary, our results highlight the homogenizing impacts of urbanization on aquatic mollusc assemblages in India, where such data are largely unavailable. These also underscore the need for long-term observations on multi-trophic impacts of urbanization would be vital for developing better environmental protection practices in India.

Acknowledgements

All authors thank the associate editor and reviewers for their comments which greatly improved the manuscript. Authors thank Yugandhar Shinde, Modern College Shivajinagar, Pune for his help and Hemant Ghate, Modern College Shivajinagar, Pune for providing the necessary literature and helping in species identification. Authors also thank N.A. Aravind, ATREE, Bangalore for his help in confirming the species identities. SMP thanks Director, Biologia Life Science LLP for her support.

Supplementary data

Supplementary data are available at JUECOL online.

Conflict of interest statement. None declared.

References