Behavioral Disturbances: The Missing Link between Sub-Organismal and Supra-Organismal Responses to Stress? Prospects Based on Aquatic Research

Abstract

Bridging the gap between early, sensitive responses to stress at the infra-organismal levels and long-term, ecologically relevant responses at the supra-organismal levels is a challenge. Behavioral ecotoxicology provides an approach that clearly links disturbances at the biochemical level (e .g., altered neurotransmitters and thyroid hormones) to effects at the population level. These effects may be direct, such as impairment of the search for a sexual partner, care of juveniles, and avoidance of predators or pollutants. Indirect effects may be alteration of reproduction success due to impairment of feeding and thus, energy metabolism. The sensitivity of behavioral responses can be useful in ecological risk assessment. A major difficulty is extrapolation of observed responses with test species to other species. Thus it is recommended to use behavioral biomarkers, associated with biochemical and physiological markers (neurotoxicity, hormones, energy metabolism) in carefully selected species. These sentinels must be key-species in the structure and functioning of ecosystems because impairments of their responses used as biomarkers will reveal a risk of cascading deleterious effects at the community and ecosystem levels.

Assessment of the health status of populations of the ragworm Nereis diversicolor using biomarkers at different levels of biological organisation

“…Links between behavioural impairment and neurotoxicity revealed by AChE inhibition are well documented for aquatic biota (Amiard-Triquet 2009). In contrast, inhibition of AChE activity was not related to burrowing activity in the present study.…”

“…Therefore it is important to study the link between the responses of biomarkers at the sub-organismal and supraorganismal levels (Forbes et al 2006). Studies of biomarkers related to energy metabolism, growth or reproduction (De Coen & Janssen 2003, Durou et al 2007b as well as behavioural disturbances (Dell'Omo 2002, Amiard-Triquet 2009) appear particularly promising. Behavioural biomarkers are sensitive tools that help us to assess the impact of contaminants at concentrations far below lethal levels.…”

Behavioural responses of the supralittoral amphipod Talitrus saltator (Montagu) to trace metals contamination

“…Different approaches have been proposed to link the responses observed at lower levels of biological organization to the effects at higher levels. Behaviour, an organismlevel response, seems to provide the most promising results (Amiard-Triquet 2009;Dell'Omo 2002 and recently revised by Hellou 2011). In fact, behavioural responses are closely related to physiological and biochemical modifications and have clear connections with population effects via alterations of reproductive success and survival (Amiard-Triquet 2009;Hellou 2011;Wallace and Estephan 2004).…”

Avoidance of contaminated sediments by an amphipod (Melita plumulosa), A harpacticoid copepod (Nitocra spinipes), and a snail (Phallomedusa solida)

“…They impact on survival [1] and affect crucial behaviors such as the ability to effectively forage for food, avoid predation, find suitable habitat, compete for resources, and tolerate a number of biotic and abiotic interactions within the surrounding environment [2]. Contaminantinduced behavioral changes can be linked to biochemical and physiological effects at the organism level, which can have flow-on effects at the population level [3]. Therefore, significant changes to crucial behavioral traits of an organism (e.g., foraging behavior, social interaction, and locomotion) may pose a threat to the survival of a population [4,5].…”

“…Behavioral traits can be exploited as toxicity test endpoints and, in some cases, have been demonstrated to be sensitive to contaminant exposure [6,7]. Consequently, behavioral endpoints are increasingly being considered to have high ecological relevance as contaminantinduced changes to an organism's behavior offer insight into potentially major environmental impacts [3]. Previous studies have reported contaminant-induced changes to a number of key behaviors, including predator-prey relationships [8], swimming and mobility [5], and contaminant avoidance [7,9].…”