Why does the larval integument of some sawfly species disrupt so easily? The harmful hemolymph hypothesis

Abstract

The larvae of several sawfly species belonging to the Tenthredinidae (Hymenoptera) have such a low mechanical resistance in the integument that slight mechanical damage to the integument is enough to provoke the release of hemolymph at a given spot. We quantified this phenomenon, which we call "easy bleeding", by measuring the pressure needed to pierce dissected sawfly integument. We also investigated the feeding deterrance of ethanolic extracts of the hemolymph by laboratory bioassays using Myrmica rubra ant workers. These traits, integument resistance and hemolymph deterrence, were inversely related, considering 22 tenthredinid species. A negative correlation was obtained by only taking into account the species of one tenthredinid tribe, namely the Phymatocerini (nine species studied). Our results support the "harmful hemolymph hypothesis" that we present here and that assumes a functional link between these morphological and chemical traits, jointly acting as a chemical defense strategy. We suspect hemolymph deterrence to be often due to sequestration of plant secondary metabolites. We discuss the role of easy bleeding, considering the fact that sawfly larvae are frequently the prey of invertebrate and vertebrate predators. It is suggested that invertebrates such as ants were more important than vertebrates in the evolution of easy bleeding.

Anti-predator defence mechanisms in sawfly larvae of Arge (Hymenoptera, Argidae)

“…Fat bodies plus salivary glands were not active and thus constituted an internal control for the other body parts tested. A large majority of tenthredinid species possess a hemolymph deterrence that is in the same order of magnitude as those in the tested Arge species (Boevé and Schaffner, 2003, Table 3). In the tenthredinids, this bioactivity is probably due to the co-occurrence of micromolecules (i.e., secondary plant metabolites) and macromolecules (e.g., proteins, with some entangling properties).…”

“…Moreover, the crude hemolymph from these larvae was pooled, then diluted and tested as well (12 replications per dilution). A deterrence rate (RD) was calculated (from Boevé and Schaffner, 2003) with the formula: RD (%) = (C -T)/(C + T), where C and T are the total number of ants feeding on the control and test droplets, respectively.…”

“…Major predators of sawfly larvae include arthropods, such as ants, and birds (Benson, 1950). Knowledge on the chemical ecology of defensive strategies in sawfly larvae mainly concerns the Diprionidae, Tenthredinidae and Pergidae (e.g., Eisner et al, 1974;Boevé and Pasteels, 1985;Wagner and Raffa, 1993;Boevé and Schaffner, 2003). In contrast, very little is known about the way Arge larvae defend against these predators, but the following traits may be involved.…”

It's Not a Bug, It's a Feature: Functional Materials in Insects

“…Biphasic secretion True bugs, [469,470] tenebrionid beetles, [638] fire ants [639] Built structures Green lacewings [640] Froths and foams Pyrgomorphid grasshoppers, [641] lubber grasshoppers, [642] froghopper nymphs [474] Hemolymph defense Sawflies, [643,644] katydids, [450,645] stoneflies, [645] stonefly nymphs [646] Projectile dispersal Stick insects, [451,459] termites [647] Material motif General functionality System of interest Insect and reference Thermoregulation Cooling Honeybees, [410] mosquitos, [411] sawflies [412] Water active properties Surface excretion Leafhoppers [166,167,648] Layering Collective materials Built structures Social wasps [649,650] Raft building to survive flooding Fire ants [580] Bivouac assemblies Army ants [512] Color vision and color manipulation Impedance matching Dragonflies, [337] cicadas, [339] butterflies, [338,341,342] moths, [342,343] beetles [342] Water active properties Desiccation resistance Antarctic midges, [651] African lake flies [652] Regular repeated patterns…”

Puncture vs. reflex bleeding: Haemolymph composition reveals significant differences among ladybird species (Coleoptera: Coccinellidae), but not between sampling methods

“…Refl ex bleeding behaviour is described for larvae and/or adults in several insect orders, e.g. Hymenoptera (Boeve & Schaffner, 2003), Plecoptera (Moore & Williams, 1990), Orthoptera (Bateman & Fleming, 2009), Hemiptera (Bugila et al, 2014) and Coleoptera (see below). Among beetles, refl ex bleeding is recorded in species belonging to sev-of the most invasive species of insect (Brown et al, 2011;Lombaert et al, 2011).…”