Removal of intensive agriculture from the landscape improves aquatic ecosystem health

https://doi.org/10.1016/j.agee.2013.05.020Get rights and content

Highlights

  • Intensive tobacco cultivation ceased in the Ovens Valley, Australia, in 2006.

  • Post-cessation, we observe reduced mentum deformities in aquatic Chironomus larvae.

  • We also observe reduced pecten epipharyngis deformities in Chironomus larvae.

  • Results suggest removal of intensive agriculture has reduced environmental stress.

  • Bioindicator results prove informative in the absence of definitive chemical data.

Abstract

The 20th century witnessed substantial increases in the intensity of agricultural land management. Increased agricultural intensity leads to degradation of aquatic ecosystems. Removal of intensive agriculture from the landscape is rare; however this occurred in the Ovens Valley, Victoria, Australia when its 150-year-old tobacco industry was closed in 2006. The present study examined stress in aquatic biota in the Ovens River and associated wetlands and dams before (1988–89) and after (2010) the tobacco closure. The endpoint observed was incidence of morphological deformities in chironomid (“non-biting midge”) larvae. A significant reduction in deformity incidence, particularly in the mentum (teeth), was observed in larvae collected from waters near or adjacent to tobacco cultivation, between 1988/89 and 2010. Similarly, there is a significant decline in the incidence of deformities in the pecten epipharyngis between 1988/89 and 2010. Ninety-six pesticides were also measured in sediments in 2010, of which only the persistent organochlorines DDT, DDE, DDD and dieldrin were detected. Some analysis of pesticides in sediments was conducted in 1988 but the results were inconclusive because the detection limits were inadequate and not all pesticides being used in tobacco cultivation at that time were analysed. The decline in morphological deformities correlates with the cessation of tobacco cultivation and indicates a recovery in ecosystem health.

Introduction

The 20th century witnessed substantial increases in the intensity of agricultural land management, much of which has been driven by policies to enhance food security and production (Dallimer et al., 2009). Globally, there has been a trend for pastoral grazing lands to be converted to intensively cultivated areas (e.g. Börjeson et al., 2008, Jones et al., 2011, Ye and Fang, 2011). Cropping and other forms of intensive cultivation are likely to have greater impacts on aquatic ecosystems than pastures because they usually involve the use of more pesticides, fertilizers and disturbance of soils (Allan, 2004). Agricultural pesticides are likely to cause degradation in stream biota (Cooper, 1993) but because pesticides are seldom measured, their environmental impact may be underrated (Skinner et al., 1997). When pesticides are monitored in receiving waters, they are often detected. In the USA, 83% of monitored streams in farmland areas had at least one pesticide for which the concentration exceeded USEPA (1986) guidelines for aquatic life (Blann et al., 2009).

Even if pesticides are detected in aquatic environments, it is difficult to understand what impact they are having on biota. This is because considering only concentrations of pesticides detected ignores possible mixture effects. When determining the impacts of pesticide pollution on aquatic organisms, it is logical to directly assess the health of exposed organisms. This can be done by conducting ecological surveys (e.g. Beketov et al., 2009) toxicity tests (e.g. Ding et al., 2011) or using biomarkers (e.g. Ramos et al., 2012). As sediments can act as a sink for pollutants (Li et al., 2000), it is important to consider sediment pollution in such toxicity tests.

Rarely is intensive agriculture removed from the landscape, but one instance of this is tobacco cultivation in Australia. Tobacco cultivation commenced in the Ovens Valley in north-eastern Victoria, Australia, during the 1850s and reached its peak production in the early 1970s (Fig. 1). During the 1980s, 3000 ha of land was still cultivated for tobacco (Rowe, 1984), however due to declining profit margins, this industry was closed in the region in 2006 (DPI, 2008).

Tobacco crops are vulnerable to a variety of pests and diseases, which require the application of large quantities of chemicals. Tobacco cultivation ranks sixth in terms of the amount of pesticide applied per unit area (U.S. General Accounting Office, 2003). Tobacco grown in the Ovens Valley was treated with a variety of pesticides, including organochlorines such as DDT and dieldrin, until they were banned in 1981 (McKenzie-Smith et al., 1994). These pesticides were replaced with organophosphates and synthetic pyrethroids.

The Environment Protection Authority of Victoria (EPA) conducted two studies of the Ovens in the late 1980s to determine if pesticides were present in streams, wetlands and dams near to and within tobacco growing regions and to determine whether there was evidence that the aquatic biota was stressed from pesticides. Organochlorine pesticides were detected in stream sediments (McKenzie-Smith, 1990).

Elevated deformities in chironomid larvae have long been associated with environmental pollution, and are considered good bioindicators of toxicant-induced stress (Warwick, 1985). Worldwide, deformities have been attributed to contamination from a variety of anthropogenic activities, including agriculture, urbanisation, mining, industry and sewage disposal (Warwick, 1985, Van Urk and Kerkum, 1987, Dermott, 1991, Dickman et al., 1992, Diggins and Stewart, 1998, Martinez et al., 2002, Bhattacharyay et al., 2005, MacDonald and Taylor, 2006, Di Veroli et al., 2012). An increased incidence of these deformities occur when the larvae are exposed to a variety of pollutants, including pesticides (Madden et al., 1992), arsenic (Martinez et al., 2006), lead and mercury (Vermeulen et al., 2000), cadmium (de Bisthoven et al., 2001). Several studies of catchments where agriculture is the dominant land use have implicated agricultural runoff as deformity-inducing (Dermott, 1991, Al-Shami et al., 2010).

Within the Murray–Darling catchment in south eastern Australia (of which the Ovens River comprises part), deformities in Procladius paludicola larvae have been associated with waters draining areas of intensive agriculture (including rice, cotton and viticulture) (Pettigrove, 1989, Townsend et al., 2009). A study investigating chironomid deformities within a rice farm in this catchment by Pettigrove et al. (1995) is perhaps the most compelling implication of agricultural chemicals. This study investigated the frequency of deformities in chironomids collected from rice bays treated with large amounts of chlorpyrifos and malathion. Significantly higher frequencies were observed in the larvae of the chironomids Polypedilum nubifer and Dicrotendipes SWL sp.1 than those from reference areas. These bays were within an agricultural property, and did not receive sewage discharge nor industrial, urban or mining runoff. Furthermore, pesticides have been shown to induce deformities in laboratory experiments on Chironomus larvae (Madden et al., 1992, Park et al., 2010, Langer-Jaesrich et al., 2010).

To infer whether the aquatic biota was stressed by pesticides, the incidence of mouthpart deformities in indigenous Chironomidae (“non-biting midge”) larvae was investigated. In the Ovens Valley study, there was a significant increase in the incidence of deformities in chironomid (genus Chironomus) larvae collected in dams, wetlands and rivers near tobacco cultivation areas than in those collected from areas upstream and more than 10 km downstream (Pettigrove, 1990).

The aim of this study was to determine whether there was evidence of a recovery in the health of the Ovens Valley aquatic ecosystems in those areas that were adjacent to and downstream of tobacco cultivation areas. A recovery in the health of the fauna would be reflected in a reduction in the incidence of chironomid mouthpart deformities compared to that reported by Pettigrove (1990). It is important to note that we did not undertake faunal surveys in this study to assess ecological metrics, but focused on the health of a bioindicator species as measured by the incidence of morphological deformities present.

Section snippets

Study area

The Ovens River Basin is located in north-east Victoria in the south-eastern region of Australia (Fig. 2) and covers an area of 7985 km2. The area extends from the Murray River in the north, to the Great Dividing Range in the south. The upper third of the Ovens catchment is forested and mountainous. The middle section comprises semi-cleared foothills and valleys, and the lower third extensively cleared riverine plains. Much of the catchment remains as intact native forests although pine

Sediment chemistry

In 1988, DDT (and/or one or both of its metabolites DDD and DDE) was detected at all three sites located within the tobacco zone but not at the upstream site (Table 3). The organochlorine pesticide endosulfan was detected at Site 9. Dieldrin, metalaxyl, organophosphates or synthetic pyrethroids were not detected at any sites.

In 2010, of the 96 pesticides analysed, only DDT, and/or its metabolites and/or dieldrin were detected in sediments from two sites in the tobacco zone, and one from the

Discussion and conclusions

The reduction in Chironomus spp. deformities observed in the tobacco zone of the Ovens Valley study area between 1988/89 and 2010 is indicative of a recovery from environmental stress.

The lack of comprehensive pesticide data corresponding to the 1988 survey limits the ability to suggest specific causative biocide/s responsible for the observed deformities. While it is clear that organochlorine pesticides were present during both surveys, it is unlikely that they were being used during this

Acknowledgements

CAPIM acknowledges funding from The Victorian Science Agenda Investment Fund managed by the Department of Business and Innovation. The authors would like to thank Gary Bennison, Graham Rooney and David Tiller for their assistance with the 1988/89 surveys and Daniel MacMahon for assistance with the 2010 field collections, chironomid identification and scoring of deformities.

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