Quantifying cryptic function loss during community disassembly

Abstract

Emerging theory suggests that the ecosystem-level consequences of anthropogenic pressures depend on how species will be disassembled from ecological communities (i.e. the disassembly rule). Species loss, however, is not the sole ecological cause of ecosystem function loss: behaviours underpinning ecosystem function can also be disrupted by anthropogenic pressures without detectable declines of component species (‘cryptic function loss’). Here, we introduce a novel framework that integrates behavioural responses into community disassembly metrics. We applied this framework to freshwater mussel communities (order Unionida) of the midwestern United States, in which intensive agricultural land use threatens stream biota. We combined a field experiment, meta-analysis and watershed-scale population dataset to assess how excessive sediment concentrations, one of the leading drivers of freshwater biodiversity loss, influence community-level water clearance rates of freshwater mussels via behavioural (changes in mass-specific clearance rate) and population (changes in population density) responses. Our study provided three key insights. First, freshwater mussels exhibited high behavioural sensitivity to increased total suspended solids (TSS) across species (i.e. reduced water clearance rate), whereas population responses were highly species-specific. Second, the behavioural response to increased TSS causes substantial cryptic function loss under stressful conditions: simulated water clearance rates when behavioural response is included can be less than half that of mussel communities with no behavioural response. Finally, simulations revealed that mussel communities are likely to show rapid but consistent rates of ecosystem function loss irrespective of disassembly rules. The similar rates of function loss are due to the uniform behavioural response to TSS that masks the linkage between population sensitivity of a species and its contribution to ecosystem function. Synthesis and applications. Our findings suggest that ignoring behavioural processes may cause non-negligible underestimation of ecosystem function loss during community disassembly, potentially leading to overly optimistic assessments of ecosystem resilience. Furthermore, unlike species declines or local extinctions, behaviour response tied to function loss may occur concurrently with increasing anthropogenic pressures. Therefore, managers should acknowledge the risk of immediate function loss after human-induced environmental changes.