On the elusiveness of enemy-free space: spatial, temporal, and host-plant-related variation in parasitoid attack rates on three gallmakers of goldenrods

Abstract

Host shifting by phytophagous insects may play an important role in generating insect diversity by initiating host-race formation and speciation. Models of the host shifting process often invoke reduced rates of natural enemy attack on a novel host in order to balance the maladaptation expected following the shift. Such "enemy-free space" has been documented for some insects, at some times and places, but few studies have assessed the occurrence of enemy-free space across years, among sites, or among insect species. We measured parasitoid attack rates on three insect herbivores of two goldenrods (Solidago altissima L. and Solidago gigantea Ait.), with data from multiple sites and multiple years for each herbivore. For each insect herbivore, there were times and sites at which parasitoid attack rates differed strongly and significantly between host plants (that is, enemy-free space existed on one host plant or the other). However, the extent and even the direction of the attack-rate difference varied strongly among sites and even among years at the same site. There was no evidence of consistent enemy-free space for any herbivore on either host plant. Our data suggest that enemy-free space, like many ecological and evolutionary forces, is likely to operate as a geographic and temporal mosaic, and that conceptual models of host shifting that include enemy-free space as a consequence of host novelty are likely too simple.

Survival, body mass and potential fecundity of the invasive moth Cameraria ohridella (Lepidoptera: Gracillariidae) on its original host plant Aesculus hippocastanum and Aesculus glabra

“…In most phytophagous insects survival and the effect of different mortality factors vary among host plants (e.g., Connor, 1991;Berdegue et al, 1996;Heard et al, 2006). In the case of C. ohridella, the causes of mortality are recorded for its original host (e.g., Grabenweger et al, 2005;Girardoz et al, 2007a, b).…”

Escape from natural enemies during climate‐driven range expansion: a case study

“…This is the most plausible explanation for all parasitoid species (except for C. astrarches ) found in the present study, as A. agestis and P. icarus feed on completely different (although sometimes growing adjacently) host plants. It is well known that plant effects can be important in limiting the extent of parasitism both of a given host species on some of its food plants ( Price et al , 1980;Gratton & Welter, 1999;Heard et al , 2006 ; and references therein) and of several host species that used different host-plants ( Geervliet et al , 2000 ). However, experimental work needs to be carried out to test this hypothesis for the present situation.…”

Detection of refuge from enemies through phenological mismatching in multitrophic interactions requires season-wide estimation of host abundance

“…Therefore, when studying the role of enemy free space, it is in some cases, notably those where phenological differences across host plants are expected, essential that data about the number of hosts are collected simultaneously with data about parasitism level. Since within-and between season variation of the impact of parasitoids can generally be high in natural systems (Scheirs and De Bruyn 2002;Heard et al 2006), it is essential that regular monitoring takes place over the entire season, and preferably even across multiple seasons (Scheirs and De Bruyn 2002).…”

“…Dozens of examples of studies involving enemy-free space can be found in the literature (Ohsaki and Sato 1994;Berdegue et al 1996;Scheirs and De Bruyn 2002;Murphy 2004;Heard et al 2006). Amongst the mechanisms generating enemy-free space, asynchrony in seasonal distribution of natural enemies and their hosts (Feder 1995) forms a prominent example.…”

“…This enabled the larvae of the apple maggot fly to develop earlier in the season, when the densities of natural enemies are still relatively low (Feder 1995). The work on Rhagoletis has inspired much other work on parasitism of phytophagous insects using different host plants (see for review Heard et al 2006), with variable success in demonstrating the existence of EFS. Typically, in such studies, the percentage of parasitism (often confusingly called ''rate'' of parasitism) of hosts living on different host plants is compared.…”