Between predators and parasitoids: Complex interactions among shelter traits, predation and parasitism in a shelter‐building caterpillar community

Abstract

1. Shelter-building is widespread in the animal world and such shelters often influence the success of their builders. Shelters built by caterpillars influence the likelihood of attacks by natural enemies, but how particular shelter traits influence caterpillar survival is not known. Furthermore, the differential effects of certain shelter traits on some natural enemies, such as predators, may lead to 'enemy-free space' for other natural enemies (parasitoids). The parasitoid enemy-free space hypothesis has not been directly tested for shelter-building caterpillars. 2. To understand how shelter traits influence caterpillar survival, shelter traits, predation and parasitism were measured simultaneously for 24 caterpillar morphospecies (1,465 caterpillars) in a tropical dry forest and analysed in a phylogenetic context. 3. Shelter type, shelter openness and whether shelters accumulated frass had different amounts of phylogenetic signal, with frass accumulation displaying the most and shelter openness the least. 4. All three traits affected the frequency with which caterpillar species experienced predation. Predation was elevated in two shelter types (leaf folds and leaf rolls) compared to cut-and-fold shelters. Combinations of shelter openness and frass accumulation also affected predation, with closed frass-free shelters having the lowest predation and closed frass-filled shelters having the highest. 5. Parasitism was not affected by shelter traits but was strongly correlated with evolutionary history and negatively correlated with predation. 6. These results confirm a trade-off between predation and parasitism and demonstrate that predation can be more frequent than parasitism. Different shelter types result in different amounts of predation. These defensive shelter traits and their effectiveness also vary phylogenetically. Together, our results suggest that predation and parasitism determine the success of shelter-building caterpillars, and that success is a function of the specific shelter they construct. More generally, our results demonstrate the importance of considering the effects of defensive traits on both predators and parasitoids when investigating interactions between herbivores and natural enemies.

Climate variability and aridity modulate the role of leaf shelters for arthropods: A global experiment

“…Conversely, herbivores might seek refuge from predators under more stable and favorable climatic conditions (Tvardikova & Novotny, 2012), where predation pressure on larger herbivores is often high (Romero et al, 2018). It is, therefore, likely that herbivores use leaf shelters more as a refuge against natural enemies (Baer & Marquis, 2020) than for protection against aridity—this hypothesis might be further tested by adding a further treatment to the experiment proposed above, that is, leaf rolls made of transpiring versus non‐transpiring material, consisting of leaf rolls with apparatus preventing predator occupancy, thereby allowing us to tease apart the respective benefits of shelter use for herbivores.…”

Enemy-Free Space for Parasitoids

“…As far back as the inception of the hypothesis parasitoids have been mentioned as potential higher trophic level species that are heavily influenced by enemy-free space (Jefferies and Lawton 1984). While little work on enemy-free space for parasitoids followed since that pivotal paper, almost all studies have found results that support the hypothesis and its predictions (Völkl 1992, Kaneko 2003, Murphy et al 2014, Baer and Marquis 2020. Ant attendance of an aphid species has been found to provide enemy-free space for both the aphid species and its primary parasitoids (Völkl 1992, Kaneko 2003.…”

“…It is noteworthy for the present study that this initial test did not distinguish these measures of parasitism and predation among caterpillar species living in the same site and year. Baer and Marquis (2020) tested the predictions of the enemy-free space hypothesis in a study of parasitoids that utilize shelter-building caterpillar hosts.…”

“…Shelter-building is a defensive phenotype of insect herbivores that is associated with increased parasitism (Hawkins 1994, Hrcek et al 2013, Baer and Marquis 2020, potentially because these semi-concealed herbivores experience less predation than exposed caterpillars, providing enemy-free space for the developing parasitoid larvae. Baer and Marquis (2020) found a negative relationship between observational measures of predation and parasitism, consistent with predictions from the enemyfree space hypothesis. This support for the enemy-free space hypothesis was contrasted with a lack of evidence for shelter traits influencing parasitism.…”

“…Many organisms face a foraging behavior trade-off between predator avoidance and increased resource acquisition; research has provided many examples of preference for habitat refuges or behaviors that provide enemy-free space at the expense of resource acquisition (e.g., Caraco et al 1980, Werner et al 1983, McPeek 1998, Persson 1993, Halpin 2000, Gonzáles et al 2001, Singer et al 2004, Moon et al 2006. Studies on insect parasitoid host use have been some of the first attempts to expand enemy-free space and apply its predictions to organisms of higher trophic levels (Völkl 1992, Kaneko 2003, Murphy et al 2014, Baer and Marquis 2020.…”