Predatory behavior and physiological response of Chinese mantids to toxic and non-toxic lepidopteran prey

Prey have evolved a number of defenses against predation, and predators have developed means of countering these protective measures. Monarch caterpillars, Danaus plexippus, for example, feed on milkweed plants in the genus Asclepias and sequester cardenolides as an anti-predator defense. However, some predators are able to consume this otherwise unpalatable prey. The observation of a Chinese mantid, Tenodera sinensis, consuming the body tissue of a monarch caterpillar while `gutting\u27 the prey (i.e., removing the gut and associated internal organs) without any apparent ill-effects prompted this research. In a series of behavioral trials we explored how adult T. sinensis handle and consume toxic (D. plexippus) and non-toxic ( Ostrinia nubilalis and Galleria mellonella) caterpillars. In addition, we analyzed differences in the C:N ratio and cardenolide content of monarch tissue consumed or discarded by mantids. We found that mantids gutted monarchs while wholly consuming non-toxic species. As expected, monarch gut tissue had a higher C:N ratio than non-gut tissue, confirming the presence of plant material. Although there were more cardenolide peaks in monarch body versus gut tissue, total cardenolide concentration and polarity index did not differ. Although T. sinensis treated toxic prey differently than non-toxic prey, gutting did not decrease the mantid\u27s total cardenolide intake. Since other predators consume monarch caterpillars whole, this behavior may be rooted in species-specific vulnerability to particular cardenolides or simply reflect a preference for high-N tissues. To further investigate the gutting behavior of the mantid, we conducted a second series of behavioral trials in which mantids were offered cardenolide-containing and cardenolide-free D. plexippus caterpillars and butterflies. In addition, we fed mantids starved and unstarved D. plexippus caterpillars from each cardenolide treatment and non-toxic Ostrinia nubilalis caterpillars. These trials were coupled with elemental analysis of the C:N ratios in gut and body tissues of both D. plexippus caterpillars and corn borers. We found that cardenolides did not affect mantid behavior: mantids gutted both cardenolide-containing and cardenolide-free caterpillars. In contrast, mantids consumed both O. nubilalis and starved D. plexippus caterpillars entirely. Danaus plexippus body tissue has a lower C:N ratio than their gut contents, while O. nubilalis have similar ratios. It is possible that the gutting behavior is in response to non-cardenolide secondary plant compound and/or an ability to regulate nutrient uptake. The results of this second suggest that while cardenolides are not driving the post-capture prey processing by mantids, it is likely driven by a sophisticated assessment of resource quality. From our first two experiments, it is clear that the Chinese mantid is able to consume cardenolide-containing monarch caterpillars, Danaus plexippus, without immediate adverse effects. Despite discarding the caterpillars\u27 gut contents, mantids still ingest cardenolides sequestered in monarch body tissue. Although mantids do not exhibit immediate adverse reactions when consuming monarch biomass, it is possible that there are long-term fitness costs associated with cardenolide consumption. We tested the hypothesis that monarch caterpillar consumption negatively affects mantid growth and reproductive condition. We assigned lab-reared mantids to one of four toxicity groups that differed in the number of monarch caterpillars offered to adult mantids over a 15-day period. Monarch consumption did not reduce mantid fecundity; all treatment groups produced similar numbers of eggs. However, mantids in the high-toxicity group produced eggs that were 42% longer on average and devoted 75% more of their biomass toward egg production than those in the control group. This increase in reproductive condition is probably driven by other factors such as mantid size, prey nutritional value and/or diet mixing. Despite consuming similar amounts of prey biomass during the experiment, mantids in the high-toxicity group gained more biomass and were larger than mantids in the other groups. These results, combined with our previous research suggest that the Chinese mantid is able to incorporate monarch prey into its diet without acute or chronic ill-effects