Detrimental effects of latex and cardiac glycosides on survival and growth of first‐instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata

Abstract

Summary1. A novel experimental method was developed to study negative physical and chemical effects of latex and cardiac glycosides on first‐instar monarch butterfly larvae in their natural environment in north central Florida. Forceps were used to nibble through the petioles of leaves of the sandhill milkweed Asclepias humistrata, mimicking the behaviour of mature monarch larvae. This notching cut off the supply of latex to the leaves without significantly reducing either their cardiac glycoside concentration or water content.2. The mean cardiac glycoside concentration in larvae that fed on intact leaves was nearly two and a half times greater than in larvae that fed on notched leaves. This was probably because more latex is present in the gut of the larvae that fed on the intact leaves. Supporting this is the fact that the mean concentration of cardiac glycosides in the latex was 34–47 times that in the leaves.3. Wet weights, dry weights, and growth rates of first‐instar larvae that fed on intact leaves over a 72‐h period were less than half those of larvae that fed on notched leaves.4. Mortality due to miring in the latex was 27% on the intact leaves compared with 2% on the notched leaves.5. Latex, cardiac glycosides, and other as yet undetermined plant factors all have a negative effect on first‐instar larval survival.6. Video‐analyses indicated that ingestion of latex caused the larvae to become cataleptic and increased their chances of being mired on the leaf by the setting latex glue. Dysfunction resulting from latex ingestion may lead to the larvae falling off the plant and being killed by invertebrate predators.7. The difficulty of neonate monarch larvae surviving on A. humistrata – one of the principal milkweed species fed on each spring as monarchs remigrate from Mexico into the southern U.S.A. – is evidence that a co‐evolutionary arms race is operating in this plant–herbivore system.

Evolutionarily stable defence and signalling of that defence

“…There is a growing body of empirical literature that demonstrates that many chemical defences incur fitness costs, either through the costs of biosynthesis or acquisition (via sequestration or symbiosis) and storage. Such costs are often seen in reductions in growth, in adult size, in fecundity or have been directly measured in energetic terms (Cohen, 1985;Zalucki et al, 2001;Bowers & Collinge, 1992;Camara, 1997;Bjorkman & Larsson, 1991;Rowell-Rahier & Pasteels, 1986;Dobler & Rowell-Rahier, 1994;Grill & Moore, 1998), although we note that in some circumstances costs have not been detected (Bowers, 1988;Kearsley & Whitham, 1992).…”

Tests of the coupled expression of latex and cardenolide plant defense in common milkweed (Asclepias syriaca)

“…Latex and cardenolides can each negatively impact specialist milkweed herbivores, including monarch butterflies (Zalucki and Malcolm 1999, Zalucki et al 2001, Agrawal 2004, Van Zandt and Agrawal 2004, Agrawal 2005, Agrawal et al 2012a, Agrawal et al 2014a), although we do not have information on their independent versus joint effects. Here we have shown that there are cardenolides in latex, but they are not concentrated compared to leaves (as is the case in other species; Seiber et al 1982, and residual latex may not contribute substantially to what we measure as ''foliar cardenolides''.…”

Phylogenetic escalation and decline of plant defense strategies

“…Three traits-cardenolides, latex, and trichomes-have been strongly implicated in providing milkweed resistance against herbivores. Each of these traits has been demonstrated to quantitatively affect the behavior (4, 5), performance (1,6,7), and abundance (8) of herbivores in the field. The resistance provided by these three traits occurs despite the fact that most milkweed herbivores are specialists and have adaptations to cope with each defense (4,5,9).…”