Cardenolide‐defended milkweed bugs do not evoke learning in Nephila senegalensis spiders

Abstract

Antipredator defense of herbivorous insects often relies on the potential toxicity of defensive chemicals sequestered from their host plants. The colorful Lygaeinae (Heteroptera: Lygaeidae) store a concentrated mixture of toxic cardenolides (cardiac glycosides) in specialized storage compartments of the bugs' integument, from which they are released upon attack. Larvae and adults of the large milkweed bug Oncopeltus fasciatus (Heteroptera: Lygaeinae) are specialized to feed on cardenolide‐containing milkweeds in the plant genus Asclepias and display a conspicuous red and black colorations. To investigate whether O. fasciatus gained improved protection by feeding on a toxic host plant (Asclepias syriaca), compared to a nontoxic alternative (sunflower seeds), we fed nymphs and adults of O. fasciatus to the golden orb‐weaver Nephila senegalensis. While visually oriented vertebrates, such as avian predators, have been intensively investigated for their reaction to defensive compounds and aposematic coloration, less attention has been paid to invertebrate predators. Their different perceptual abilities can provide important opportunities for testing hypotheses on warning coloration and chemical defenses. The predation trials showed that the bugs fed on Asclepias were significantly less likely to be killed than the bugs reared on a cardenolide‐free diet. This suggests that sequestered cardenolides in O. fasciatus nymphs and adults represent a significant fitness advantage on an individual level against this invertebrate predator. Yet, when testing for avoidance learning in the spiders, negative experience did not change the way how similar prey was attacked at the next encounter. In this case, visual or chemical aposematism thus does not seem to matter for predator learning.

Testing the effectiveness of pyrazine defences against spiders

“…While the spiders did take longer to attack wood tiger moths in comparison to their usual fly prey, this may have been because the moths moved less in the web than the flies. Alternatively, it may be that the spiders were more cautious when attacking unfamiliar prey (but see Bramer et al 2018). In addition, the spiders spent more time wrapping the moths, and ate a smaller proportion of their body weight compared to the flies, although this was probably a result of the larger wings of the moths.…”

“…The results of a limited number of trials with the smaller European species L. sclopetarius suggest the moths are palatable even to smaller spiders, but that the size of the moths, and difficulties handling them, may be enough to provide some protection, as two individuals were released by bridge spiders (see Supplementary materials). In addition, while actively hunting spiders have been shown to learn to avoid aposematic prey (McIver and Lattin 1990) it is far less clear if web-building spiders can do the same (Bramer et al 2018), particularly as they are unlikely to use visual cues, such as colour. Without avoidance learning these spiders can only taste-reject prey, which may also reduce the benefit of chemical defences against them.…”

Intraspecific variation in responses to aposematic prey in a jumping spider (Phidippus regius)

“…The cardenolides present in milkweed bugs have been well studied and are highly toxic to vertebrates (Seiber, Lee, & Benson, 1983) and have even shown some degree of toxicity to the congener Phidippus audax when artificially delivered (via cardenolide‐treated fruit flies, see Hill, 2006). However, the natural toxicity of milkweed bugs to invertebrate predators has been difficult to ascertain because the invertebrate predators that have been studied typically reject them as prey items (or regurgitate them) due to their unpalatability (Berenbaum & Miliczky, 1984; Bramer et al., 2018; Hill, 2006; Paradise & Stamp, 1991; Skow & Jakob, 2006; Taylor et al., 2016). Our results here suggest that more work is needed to understand how both palatability and toxicity may (or may not) affect the diverse suite of arthropod predators that encounter them in the field.…”

“…Previous studies with Phidippus jumping spiders report that the spiders always reject milkweed bugs after attack, and will wipe their mouthparts on the substrate after rejecting them (Hill, 2006). Recent work with the golden orb‐web spider, Nephila senegalensis , found that milkweed bugs were almost always rejected and released unharmed; following a test bite, spiders would reject them, cut them out of the web and clean their mouthparts (Bramer, Schweizer, & Dobler, 2018). These findings suggest that milkweed bugs are unpalatable and likely have toxic effects on these predators; yet because none of these predators are willing to consume the bugs, we know little about how these toxins would affect individual predators if they did choose to consume them.…”

Defense of Milkweed Bugs (Heteroptera: Lygaeinae) against Predatory Lacewing Larvae Depends on Structural Differences of Sequestered Cardenolides

“…Moreover, spiders built disrupted webs when feeding on toxic aphids [ 36 ]. Similarly, Asclepias seed-fed adults and nymphs of O. fasciatus were significantly less likely to be preyed upon by Nephila senegalensis spiders than control bugs raised on sunflower seeds [ 37 ]. Even the eggs of milkweed-raised females of O. fasciatus , that are known to contain cardenolides via maternal transfer [ 38 ], were found to be protected against the larvae of the lacewing Chrysoperla carnea [ 39 ].…”