Comparative Functional Responses Predict the Invasiveness and Ecological Impacts of Alien Herbivorous Snails

Abstract

Understanding determinants of the invasiveness and ecological impacts of alien species is amongst the most sought-after and urgent research questions in ecology. Several studies have shown the value of comparing the functional responses (FRs) of alien and native predators towards native prey, however, the technique is under-explored with herbivorous alien species and as a predictor of invasiveness as distinct from ecological impact. Here, in China, we conducted a mesocosm experiment to compare the FRs among three herbivorous snail species: the golden apple snail, Pomacea canaliculata, a highly invasive and high impact alien listed in “100 of the World's Worst Invasive Alien Species”; Planorbarius corneus, a non-invasive, low impact alien; and the Chinese native snail, Bellamya aeruginosa, when feeding on four locally occurring plant species. Further, by using a numerical response equation, we modelled the population dynamics of the snail consumers. For standard FR parameters, we found that the invasive and damaging alien snail had the highest “attack rates” a, shortest “handling times” h and also the highest estimated maximum feeding rates, 1/hT, whereas the native species had the lowest attack rates, longest handling times and lowest maximum feeding rates. The non-invasive, low impact alien species had consistently intermediate FR parameters. The invasive alien species had higher population growth potential than the native snail species, whilst that of the non-invasive alien species was intermediate. Thus, while the comparative FR approach has been proposed as a reliable method for predicting the ecological impacts of invasive predators, our results further suggest that comparative FRs could extend to predict the invasiveness and ecological impacts of alien herbivores and should be explored in other taxa and trophic groups to determine the general utility of the approach.

Assessing the ecological impacts of invasive species based on their functional responses and abundances

“…Alexander et al 2014a, b;Dick et al 2013Dick et al , 2017Paterson et al 2014;Laverty et al 2015;Xu et al 2016) have shown that the comparative FR methodology is rapid, efficient and effective at explaining and predicting the ecological damage caused by invasive species. However, in some cases the FR of invasive species is unremarkable when compared to those of native species, yet ecological damage is known to occur, as is the case with N. melanostomus and P. parva toward invaded communities (Barton et al 2005;Britton et al 2010;Gozlan et al 2010;Pagnucco and Ricciardi 2015).…”

“…However, recent comparisons of invader and native functional responses (FRs) have often yielded excellent explanatory and predictive power of invader impact on native prey populations (Alexander et al 2014a, b;Dick et al 2013Dick et al , 2014Dick et al , 2017, and this has recently been extended to damaging herbivorous invaders (e.g. golden apple snail; Xu et al 2016). Indeed, the method is applicable to any taxonomic or trophic group due to the universal nature of organisms utilizing resources (Dick et al 2017).…”

“…bloody red shrimp Hemimysis anomala, Dick et al 2013; largemouth bass Micropterus salmoides, Alexander et al 2014a, b; killer shrimp Dikerogammarus villosus, Dodd et al 2014; golden apple snail Pomacea canaliculata Xu et al 2016); these invasive consumers show significantly higher FRs than trophically analogous native consumers. However, ecological impacts, such as by predators, will be the product of their per capita effects and the number of individuals having those effects; both must be quantified to elucidate overall effects.…”

Functional responses can unify invasion ecology

“…For example, while most invader/native functional response comparisons to date have examined predator-prey systems (e.g. Dick et al 2013), there are emerging studies involving herbivore-plant (Xu et al 2016) and plant-nutrient interactions (see RossiterRachor et al 2009). The latter study, by using completely different terminologies, led to the existence of essentially similar thinking by animal and plant invasion scientists-who, thus far, have had little collaborative interaction or consideration of each other's research.…”

“…in ballast water tanks) and become established in new locations-where resources might be in short supply or already being utilised by existing native species. Similarly, invader establishment and spread may be facilitated by resource use patterns, again measurable by functional response studies, and species invasiveness as distinct from ecological impact (see Ricciardi and Cohen 2007) may also be correlated with functional responses (see Bovy et al 2015;Xu et al 2016). One aspect that might considerably improve the use of functional responses in such contexts would be incorporation of abundance, as per Parker et al (1999), which is essentially the numerical response that, together with the functional response, gives the total response (or total uptake rate; see Dick et al 2014).…”