Secondary Defense Chemicals in Milkweed Reduce Parasite Infection in Monarch Butterflies, Danaus plexippus

Abstract

In tri-trophic systems, herbivores may benefit from their host plants in fighting parasitic infections. Plants can provide parasite resistance in two contrasting ways: either directly, by interfering with the parasite, or indirectly, by increasing herbivore immunity or health. In monarch butterflies, the larval diet of milkweed strongly influences the fitness of a common protozoan parasite. Toxic secondary plant chemicals known as cardenolides correlate strongly with parasite resistance of the host, with greater cardenolide concentrations in the larval diet leading to lower parasite growth. However, milkweed cardenolides may covary with other indices of plant quality including nutrients, and a direct experimental link between cardenolides and parasite performance has not been established. To determine if the anti-parasitic activity of milkweeds is indeed due to secondary chemicals, as opposed to nutrition, we supplemented the diet of infected and uninfected monarch larvae with milkweed latex, which contains cardenolides but no nutrients. Across three experiments, increased dietary cardenolide concentrations reduced parasite growth in infected monarchs, which consequently had longer lifespans. However, uninfected monarchs showed no differences in lifespan across treatments, confirming that cardenolide-containing latex does not increase general health. Our results suggest that cardenolides are a driving force behind plant-derived resistance in this system.

Effects of phenological synchronization on caterpillar early-instar survival under a changing climate

“…On A. syriaca, a plant with low cardenolide content, larvae protected in cages had a higher survival rate (92%) than larvae left free on plants (24%) (Zalucki et al 2001b). Adding cardenolides to the artificial diet fed to monarch caterpillars infected with O. elektroscirrha slowed parasite growth and increased lifespan of infected but not uninfected butterflies (Gowler et al 2015). Cardenolide consumption thus appears to mediate a trade-off between toxicity and protection.…”

Host Diet Affects the Morphology of Monarch Butterfly Parasites

“…Previous studies have shown that infected monarchs reared on milkweeds with high cardenolide concentrations exhibit reduced parasite loads and increased tolerance to parasites (de Roode et al, 2008a(de Roode et al, , 2011aLef`evre et al, 2010;Sternberg et al, 2012;Gowler et al, 2015;Tao et al, 2015Tao et al, , 2016. Cardenolides may cause these reductions in parasite loads by increasing host immunity to the parasite, as has been seen in other systems (Lee et al, 2008;Povey et al, 2009;Simpson et al, 2015), or by direct inhibition of parasites (Cory and Hoover, 2006).…”

“…Many previous studies have documented the antimicrobial, antiviral, anti-parasitic, and anti-cancer qualities of plant secondary chemicals (Ohigashi et al, 1992;Murakami et al, 1994Murakami et al, , 1996Billing and Sherman, 1998;Sherman and Billing, 1999). In the monarch-parasite system, infected monarch butterflies have shown decreases in parasite loads and increases in tolerance to O. elektroscirrha when reared on milkweeds with higher cardenolide concentrations (de Roode et al, 2008a(de Roode et al, , 2011bSternberg et al, 2012;Gowler et al, 2015;Tao et al, 2015Tao et al, , 2016. Although the medicinal qualities of numerous plant chemicals are clear (Hunter, 2016), their direct effects on parasite morphology, as well as any related effects on pathogenicity and transmission, are unknown (Okagaki et al, 2010;Zaragoza et al, 2010).…”

“…Monarchs are specialized on milkweeds and can sequester cardenolides for their own defense against predators (Brower, 1969). Previously, it has been shown that infected monarchs reared on milkweeds with high cardenolide concentrations exhibit both a reduced parasite load and longer lifespan compared to infected monarchs reared on milkweeds with low cardenolide concentrations (de Roode et al, 2008a;Sternberg et al, 2012;Gowler et al, 2015;Tao et al, 2015). Moreover, infected female butterflies prefer to lay eggs on high-cardenolide milkweed in 2-species choice tests, thereby reducing infection and disease in their offspring (Lef`evre et al, 2010.…”

Assessing Role of Major Drivers in Recent Decline of Monarch Butterfly Population in North America

“…Higher levels of cardenolides in milkweed species could lower O. elektroscirrha infestation. For instance, monarch larvae reared on A. tuberosa, feeding on higher doses of cardenolides resulted in lower parasite infestation of their pupae (Gowler et al, 2015).…”