2100 Environmental Toxicology and Chemistry, Vol. 19, No. 8, pp. 2100–2106, 2000 2000 SETAC Printed in the USA 0730-7268/00 $9.00 + .00 TOWARD A MECHANISTIC UNDERSTANDING OF CONTAMINANT-INDUCED CHANGES IN DETRITUS PROCESSING IN STREAMS: DIRECT AND INDIRECT EFFECTS ON DETRITIVORE FEEDING DAVID M. FORROW*² and L ORRAINE MALTBY‡ ²Environment Agency, National Centre for Ecotoxicology and Hazardous Substances, Howbery Park, Wallingford, Oxfordshire OX10 8BD, United Kingdom ‡Department of Animal and Plant Sciences, The University of Sheffield, Sheffield, S10 2TN, United Kingdom ( Received 27 July 1999; Accepted 11 January 2000) Abstract—Macroinvertebrate feeding is a major rate-limiting step in the processing of detritus in streams. Environmental contam- inants can reduce detritus processing by decreasing the abundance or feeding activity of detritivores. Contaminant-induced reductions in detritus processing can have important consequences for the structure and functioning of the stream community. Here we investigate the mechanistic basis for reduced leaf processing in a stream contaminated with motorway (superhighway) runoff. In situ and laboratory studies were used and the work focused on Gammarus pulex (Amphipoda), the dominant detritivore at the site. The in situ feeding rate of G. pulex was significantly reduced downstream of the motorway discharge. Reductions in feeding rate could be the result of contaminants in the discharge having a direct effect on the animal or the discharge may affect the animal’s feeding indirectly, by reducing food quality. Food quality may be reduced by contaminant accumulation or changes in microbial conditioning. Laboratory studies demonstrated that the main mechanism responsible for the reduction in feeding was direct toxicity and that this was most severe when animals were in direct contact with contaminated sediments. Neither contaminant accumulation nor differences in microbial conditioning affected the choice or consumption of leaf material by G. pulex over short exposure periods (i.e., 14 d). However, contaminant-induced reductions in microbial conditioning were important over longer exposure periods (i.e., 27 d). Keywords—Feeding Gammarus pulex Leaf processing Motorway runoff Sediment toxicity INTRODUCTION The decomposition of detrital material is an important pro- cess in freshwaters and may account for more than 99% of the annual energy budget of small streams [1,2]. The break- down of leaf material in streams is brought about by a com- bination of chemical leaching, microbial decomposition (pri- marily by aquatic hyphomycetes), macroinvertebrate feeding, and physical abrasion [3]. These processes are not independent. For instance, microbial decomposition of leaf material makes it more palatable to macroinvertebrates [4] and therefore more prone to consumption. Macroinvertebrate feeding, a major rate-limiting step in the processing of the leaf material in aquat- ic systems [5], can be reduced by exposure to environmental contaminants [3,6]. Toxicant-induced reductions in feeding rate can result in reduced growth, size, fecundity, and survival of individuals [7–10]. In addition, reductions in leaf processing and consequent effects on detritivore populations can result in changes in the structure of the stream community [11]. Runoff from road surfaces contains a large number of con- taminants that may have adverse effects on the biota of re- ceiving waters [12,13]. These effects are most severe when runoff from large, heavily used roads such as motorways (su- perhighways) discharge into small streams [13]. In a previous paper we described the effects of runoff from British motor- ways on the environmental quality and ecology of receiving waters [13]. Sites receiving motorway runoff had elevated sed- iment concentrations of hydrocarbons and heavy metals and elevated water concentrations of heavy metals and selected * To whom correspondence may be addressed (david.forrow@environment-agency.gov.uk). anions. Further, a change occurred in the composition and diversity of the benthic macroinvertebrate assemblage in four of the seven streams surveyed. These effects were most marked at the point where runoff from a heavily used section of the M1 motorway entered a small stream, Pigeon Bridge Brook, as a point source discharge. Input of motorway runoff into Pigeon Bridge Brook was also associated with a reduction in the breakdown of leaf material caused by a decrease in ma- croinvertebrate-mediated processes [13]. Reductions in the processing of leaf litter by macroinver- tebrates result from a reduction in their abundance or feeding activity. Detritivores that feed on coarse particulate organic material such as leaf litter are known as shredders (sensu [14]). The abundance of the major shredder in Pigeon Bridge Brook, Gammarus pulex, was reduced below the motorway discharge [13] and here we investigate the effect of motorway runoff on the feeding activity of G. pulex. In particular, we ask how exposure to runoff-contaminated water and sediment affects the consumption of leaf material by G. pulex and what mech- anistic bases these effects have. Contaminants may affect the feeding of shredders directly, through changes in behavior or physiology, or indirectly through changes in food quality resulting from alterations in microbial colonization and decomposition or contaminant ac- cumulation [6,15–17]. In situ deployments were used to in- vestigate the effects of motorway runoff on Gammarus feeding rate (experiment 1) and to assess whether pre-exposure of leaf material to motorway contaminants affected its subsequent utilization by G. pulex (experiment 2). In addition, a series of laboratory experiments was designed to distinguish between direct and indirect effects and to identify the mechanisms by which motorway runoff affects G. pulex feeding.