Scrutinizing the enemy release hypothesis: population effects of parasitoids on Harmonia axyridis and local host coccinellids in Brazil

Abstract

The Enemy Release Hypothesis (ERH) has been a factor influencing the establishment of some exotic species worldwide. We tested if the ERH could be influencing populations of the exotic predator Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) in Brazil. During two years, three local predatory coccinellid species and Harmonia axyridis were sampled in Brassica oleracea in six organic farms in the midwest of the country. Parasitoids were detected by rearing (emerged) and qPCR Melting Curve Analysis (unemerged). Host density-dependence and spillovers were used to evaluate coccinellid population effects of parasitism. Six parasitoid species were found, including two new records for Brazil. Although Harmonia axyridis harbored fewer parasitoid species, parasitism was not lower and parasitoid densitydependence was not weaker on it compared to the local species. Spillovers among hosts occurred both onto Harmonia axyridis and from it. The ERH was rejected for these parasitoids and, therefore, it did not contribute to the invasiveness of Harmonia axyridis in Brazil.

The invasive coccinellid Harmonia axyridis (Coleoptera: Coccinellidae) is a less suitable host for parasitism than resident species

“…Therefore, our study is the first report of low suitability in the field in South America and is confirmed by the results of laboratory tests. This, together with the results obtained in laboratory studies in Curitiba in Brazil (Castro-Guedes & Almeida, 2016), but not from field studies in the Distrito Federal in Brazil (Paula et al, 2020), indicate that at least two independent introductions of this invasive alien species to South America from eastern North America (Lombaert et al, 2014) have occurred, corresponding to populations that could better escape this natural enemy in comparison to other resident species (native or introduced). Therefore, even though the adaptation of natural enemies to novel invasive species is thought to occur by the ERH, in Chile, to date, D. coccinellae populations have not developed a strong ability to parasitize H. axyridis, contrary to what has occurred in some European populations that have had a longer period of interaction (Dindo et al, 2016;Knapp et al, 2019).…”

“…Another possibility is that in the field, parasitoids attack larvae, which are less mobile and may be less aggressive than adults and therefore are less likely to escape from the parasitoid. In fact, studies have shown that even though adult coccinellids are the stage most attacked by D. coccinellae, fourth and third instar larval stages are also parasitized (Firlej, Boivin, Lucas, & Coderre, 2005;Obrycki et al, 1985;Paula et al, 2020). The fourth and third instar larvae of H. axyridis would also be more susceptible to parasitoid oviposition than adults, since they have less aggressive defensive behavior (Berkvens et al, 2010;Firlej et al, 2005Firlej et al, , 2010Hoogendoorn & Heimpel, 2002).…”

“…Parasitism by D. coccinellae can vary depending on host species, location and time since invasion, among other factors, due to genetic differences between species or populations and the adaptation of the parasitoid to the new host (Ceryngier et al, 2017(Ceryngier et al, , 2012Knapp et al, 2019;Paula et al, 2020). The complexity of different interactions in the field, in turn mediated by the abundance of coccinellid species and parasitoids, could modulate the parasitism rate by this natural enemy, so laboratory experiments are an important complement to field assessments to better understand this process.…”

“…The lower suitability of H. axyridis for the parasitoid has been explained by several mechanisms involving behavior, the immune system and physiology (Firlej, Girard, Brehélin, Coderre, & Boivin, 2012;Firlej, Lucas, Coderre, & Boivin, 2007. However, in some invaded regions, H. axyridis has the same or even greater rates of successful parasitism by D. coccinellae than resident species (Dindo et al, 2016;Knapp et al, 2019;Paula et al, 2020). Some authors have drawn attention to the dynamism of biological invasions, expecting an adaptation by natural enemies to invasive species over time (Knapp et al, 2019;Roy, Lawson Handley, Schönrogge, Poland, & Purse, 2011).…”

“…In South America, where H. axyridis invaded more recently than in North America (Lombaert et al, 2014), only one study under laboratory conditions in Brazil assessed the relative parasitism of H. axyridis compared to that of other coccinellid species, finding that the invader is a poor host for D. coccinellae (Castro-Guedes & Almeida, 2016). However, in a more recent field study in a different region of Brazil, H. axyridis suffered equal or more parasitism by D. coccinellae than other resident species (Paula et al, 2020). However, these results do not necessarily apply to other regions of the continent, such as Chile, since Brazilian and Chilean H. axyridis populations are genetically different (Lombaert et al, 2014), as the parasitoid populations may also be.…”