Plant species with higher chemical defences enhance herbivore cellular immunity with differential effectiveness against two parasitoid species

Abstract

1. Insect herbivores simultaneously experience bottom-up effects of plant defensive chemistry and the top-down effects of natural enemies. At the intersection of these effects are herbivore immune systems, herbivore traits that have largely been overlooked in studies of plant-insect interactions. Most previous studies have demonstrated compromised immunity of herbivores that feed on plants with higher defensive chemistry. Many studies have used embedded microfilaments or silica beads as proxies for parasitoid eggs. Yet, parasitoids may evade or suppress host immune responses by injecting venom and calyx fluid, or through modifications of their egg surface structure, necessitating studies that include all three trophic levels to obtain a complete picture of how plant traits may modulate herbivore immunity.2. Here, we examined the effect of host plant species that differ in glucosinolate (antiherbivore compounds produced by plants in the Brassicaceae) concentrations on the immune status of an herbivore and its consequences for two species of parasitoids with different life history traits.3. We found that larvae of the butterfly Pieris rapae that fed on field mustard Brassica rapa, which contain 52-fold higher glucosinolate concentrations than collards B. oleracea, attained lower body weights and experienced prolonged development to adulthood.4. Yet, caterpillars that fed on B. rapa had enhanced cellular immunity, as measured by total and differential haemocyte counts as well as melanization capacity, compared to larvae that fed on B. oleracea. 5. In turn, the likelihood that at least some eggs in clutches of the gregarious endoparasitoid Cotesia glomerata would be encapsulated, leading to a reduction in brood size, were three times greater when their host caterpillars fed on B. rapa compared to B. oleracea.6. Interestingly, eggs of the solitary endoparasitoid Cotesia rubecula were rarely encapsulated irrespective of the host plant on which their host caterpillar fed. | 1493Functional Ecology GHOSH et al. | Study organismsSeeds of collards (Brassica oleracea var. viridis) and field mustard (Brassica rapa subsp. dichotoma) were obtained from the USDA-GRIN seed bank. All plants were grown under greenhouse conditions (26 ± 8°C, 40%-60% RH, and a L:D 16:8 h photoperiod) in 20 cm diameter pots filled with potting soil (Lambert LM-HP) and 5 g of Osmocote fertilizer (N: P: K -1: 1: 1). After 4 weeks, plants with four to six fully expanded leaves were used for all experiments. Adult P. rapae were collected from an organic crucifer farm near Fort Collins, Colorado. Cotesia glomerata cocoons were collected from the same crucifer fields near Fort Collins, and C. rubecula colonies were started from cocoons collected on crucifers on the University of Minnesota campus in St. Paul, Minnesota. Both parasitoid colonies were maintained by parasitizing second instar P. rapae larvae. These colonies were periodically supplemented with fieldcollected parasitoids. Adult parasitoids were maintained in humiditycontrolled incubator (15°C, 50...

The plant toxin 4-methylsulfinylbutyl isothiocyanate decreases herbivore performance and modulates cellular and humoral immunity

“…These observations suggest a possible difference between generalist and specialist herbivores. Previous studies on the specialist caterpillars Plutella xylostella and Pieris rapae have shown that higher glucosinolate concentrations are correlated with enhanced cellular immunity against parasitic wasps at the cost of reduced larval weight and development success [ 10 , 30 ]. Although, T .…”

“…Hence, along with the ability to cope with plant toxins, caterpillars must also defend against their natural enemies to successfully survive. Previous research has shown a direct correlation between plant toxins and caterpillar immune responses [ 8 – 10 ]. For example, plant defense metabolites like catalpol and other iridoid glycosides suppress the immunocompetence of sequestering species such as Junonia coenia (Lepidoptera: Nymphalidae) and Ceratomia catalpa (Lepidoptera: Sphingidae) [ 7 , 11 ].…”

“…For example, plant defense metabolites like catalpol and other iridoid glycosides suppress the immunocompetence of sequestering species such as Junonia coenia (Lepidoptera: Nymphalidae) and Ceratomia catalpa (Lepidoptera: Sphingidae) [ 7 , 11 ]. On the other hand, glucosinolates have been shown to enhance the immune system of specialist herbivores that detoxify plant toxins such as Plutella xylostella (Lepidoptera: Plutellidae) and Pieris rapae (Lepidoptera: Pieridae) [ 10 , 12 ]. In addition, studies have demonstrated that pyrrolizidine alkaloids enhance the survival of Grammia incorrupta caterpillars against parasitoids [ 13 ].…”

Volatiles from cotton aphid (Aphis gossypii) infested plants attract the natural enemy Hippodamia variegata

“…When a plant is exposed to HIPVs from a neighboring plant that is being attacked by herbivores, the plant will begin to produce its own defenses in preparation for a possible attack. This priming process can help to reduce the amount of damage that the plant sustains if it is attacked by herbivores ( Turlings and Erb, 2018 ; Ghosh et al., 2023 ).…”