Searching behaviour of an omnivorous predator for novel and native host plants of its herbivores: a study on arthropod colonization of eucalyptus in Brazil

Abstract

Adaptation to novel host plants is a much-studied process in arthropod herbivores, but not in their predators. This is surprising, considering the attention that has been given to the role of predators in host range expansion in herbivores; the enemy-free space hypothesis suggests that plants may be included in the host range of herbivores because of lower predation and parasitism rates on the novel host plants. This effect can only be important if natural enemies do not follow their prey to the novel host plant, at least not immediately, thus allowing the herbivores to adapt to the novel host plant. Hence, depending on the speed with which natural enemies follow their prey to a new host plant, enemy-free space on novel host plants may only exist for a limited period. This situation may presently be occurring in a system consisting of the herbivorous moth Thyrinteina arnobia Stoll (Lepidoptera: Geometridae) that attacks various species of Myrtaceae, such as guava ( Psidium guajava L.) and jaboticaba ( Myrciaria spp.), in Brazil. Since the introduction of eucalyptus (Myrtaceae) species into this country some 100 years ago, the moth has included this plant species in its host range and frequently causes outbreaks, a phenomenon that does not occur on the native host plant species. This suggests that the natural enemies that attack the herbivore on native species are not very effective on the novel host. We tested this hypothesis by studying the searching behaviour of one of the natural enemies, the omnivorous predatory bug Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae). When offered a choice between plants of the two species, the predators (originally collected in eucalyptus plantations) preferred guava to eucalyptus when both plant species were clean, infested with herbivores, or damaged by herbivores but with herbivores removed prior to the experiments. The bugs preferred herbivore-damaged to clean guava, and showed a slight preference for damaged to clean eucalyptus. These results may explain the lack of impact of predatory arthropods on herbivore populations on eucalyptus and suggests that eucalyptus may offer an enemy-free space for herbivores.

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

“…For example, the shift by the apple maggot fly, Rhagoletis pomonella, from hawthorn to apple affords escape from parasitoids because the size of apples lets flies feed far deeper inside fruits than parasitoid ovipositors can reach (Feder 1995; see also Gruenhagen and Perring 2001;Oppenheim and Gould 2002). In contrast, if a novel host offers EFS only because it is novel and there is a lag in the evolution of parasitoid or predator searching behavior, then EFS might represent only a transitory phase in host shifting (Grosman et al 2005). Such transitory EFS might not Nason et al (2002) be easily detectable, but could still be critical to host shifting and the rapid evolution of distinct, genetically isolated host forms.…”

The Gall MidgeAsphondylia borrichiae(Diptera: Cecidomyiidae): An Indigenous Example of Host-Associated Genetic Divergence in Sympatry

“…Interestingly, the acquisition of "enemy-freespace" has been proposed as trade-off for reduced larval performance on non-natal host plants since parasitism is initially lower after establishment on a new plant (Mira & Bernays 2002;Murphy 2004;Grosman et al 2005). However, once the parasitoids incorporate a novel plant into their search image parasitism rates will increase (reviewed by Ishii & Shimada 2010); and, if the development times of the gall midge are asynchronous (as is the case in this system), cascading HAD of populations of both the midge and its parasitoids may develop in sympatry.…”

Antibiosis of Eucalyptus plants on Podisus nigrispinus

“…Hence, this is one possible cause for the lower survival of this predator on eucalyptus, which has been considered as due to phytophagy compared with guava. P. nigrispinus showed lower colonization of P. nigrispinus fed on Thyrinteina arnobia reared with eucalyptus than guava, which was attributed to qualitative differences of prey in two host plants, possibly due to toxic compounds in eucalyptus that could be sequestered by their prey and affect the third trophic level (Grosman et al 2005). Chemical defense of plants generally has a negative impact on the characteristics of natural enemies, such as growth, development, survival and morphology of predators and parasitoids (De Clercq et al 2000;Havill and Raffa 2000;Ode et al 2004).…”