Paul K. Abram

An Insect with Selective Control of Egg Coloration

The color and patterning of animal eggs has important consequences for offspring survival. There are examples of between-species and polymorphic differences in egg coloration in birds and amphibians [1-3], as well as cases of birds and insects whose nutritional status or age can cause within-individual variation in egg pigmentation [4-6]. However, no studies to date have demonstrated that individual animals can selectively control the color of their eggs. Here, we show that individual females of the predatory stink bug Podisus maculiventris can control the pigmentation of their eggs during oviposition, as a response to environmental conditions. The color of egg masses produced by individual females can range from pale yellow to dark black/brown. Females tend to lay darker eggs, which are more resistant to UV radiation, on the upper surface of leaves where UV exposure is highest in nature. Conversely, they lay lighter eggs on the undersides of leaves. However, egg color is not determined by the intensity of UV radiation falling on the surface where they are laid. Rather, female stink bugs appear to use a visual assessment of oviposition substrate reflectance to determine egg color. Unexpectedly, biochemical analyses revealed that the egg pigment is not melanin, the most ubiquitous light-absorbing pigment in animals. Our study offers the first example of an animal able to selectively control the color of its eggs.

Increasing host age does not have the expected negative effects on the fitness parameters of an egg parasitoid

Host age is an important determinant of host acceptance and suitability for egg parasitoids. As host embryonic development advances, the quality of resources available to the parasitoid offspring typically declines, usually resulting in reduced acceptance levels by foraging females and lower offspring fitness. We examined the ability of the parasitoid Telenomus podisi Ashmead (Hymenoptera: Scelionidae) to parasitize and develop in Podisus maculiventris (Say) (Hemiptera: Pentatomidae) eggs of different ages. In laboratory experiments, we measured the effect of host age (6, 24, 48, 72, 96, or 120 h old) on parasitism rate and offspring fitness parameters such as survival, development time, sex ratio, and size. Contrary to our expectations, parasitism rate did not differ between host age treatments, nor did sex ratio allocation, offspring size, or the fecundity of newly emerged female offspring. However, parasitoid offspring had a longer development time with increasing host age. This trend was stronger for males than for females, which we suggest could reduce the degree of protandry among offspring emerging from older host eggs, thus increasing the rate of virginity upon leaving the emergence patch and resulting in more frequent off‐patch mating by female offspring in nature. Overall, our results suggest that all stages of P. maculiventris embryonic development are suitable for acceptance and development of T. podisi. Unlike most species of egg parasitoids, T. podisi has evolved mechanisms to utilize host resources, regardless of host developmental stage, with relatively minor fitness consequences.

A scenario for the evolution of selective egg coloration: the roles of enemy-free space, camouflage, thermoregulation and pigment limitation

Behavioural plasticity can drive the evolution of new traits in animals. In oviparous species, plasticity in oviposition behaviour could promote the evolution of new egg traits by exposing them to different selective pressures in novel oviposition sites. Individual females of the predatory stink bug Podisus maculiventris are able to selectively colour their eggs depending on leaf side, laying lightly pigmented eggs on leaf undersides and more pigmented eggs, which are more resistant to ultraviolet (UV) radiation damage, on leaf tops. Here, we propose an evolutionary scenario for P. maculiventris egg pigmentation and its selective application. We experimentally tested the influence of several ecological factors that: (i) could have favoured a behavioural shift towards laying eggs on leaf tops and thus the evolution of a UV-protective egg pigment (i.e. exploitation of enemy-reduced space or a thermoregulatory benefit) and (ii) could have subsequently led to the evolution of selective pigment application (i.e. camouflage or costly pigment production). We found evidence that a higher predation pressure on leaf undersides could have caused a shift in oviposition effort towards leaf tops. We also found the first evidence of an insect egg pigment providing a thermoregulatory advantage. Our study contributes to an understanding of how plasticity in oviposition behaviour could shape the responses of organisms to ecological factors affecting their reproductive success, spurring the evolution of new morphological traits.

Influence of temperature on patch residence time in parasitoids: physiological and behavioural mechanisms.

Patch time allocation has received much attention in the context of optimal foraging theory, including the effect of environmental variables. We investigated the direct role of temperature on patch time allocation by parasitoids through physiological and behavioural mechanisms and its indirect role via changes in sex allocation and behavioural defences of the hosts. We compared the influence of foraging temperature on patch residence time between an egg parasitoid, Trichogramma euproctidis, and an aphid parasitoid, Aphidius ervi. The latter attacks hosts that are able to actively defend themselves, and may thus indirectly influence patch time allocation of the parasitoid. Patch residence time decreased with an increase in temperature in both species. The increased activity levels with warming, as evidenced by the increase in walking speed, partially explained these variations, but other mechanisms were involved. In T. euproctidis, the ability to externally discriminate parasitised hosts decreased at low temperature, resulting in a longer patch residence time. Changes in sex allocation with temperature did not explain changes in patch time allocation in this species. For A. ervi, we observed that aphids frequently escaped at intermediate temperature and defended themselves aggressively at high temperature, but displayed few defence mechanisms at low temperature. These defensive behaviours resulted in a decreased patch residence time for the parasitoid and partly explained the fact that A. ervi remained for a shorter time at the intermediate and high temperatures than at the lowest temperature. Our results suggest that global warming may affect host-parasitoid interactions through complex mechanisms including both direct and indirect effects on parasitoid patch time allocation.

Potential impact of the native hyperparasitoid Conura albifrons (Hymenoptera: Chalcididae) on the exotic biological control agent Diadromus pulchellus (Hymenoptera: Ichneumonidae)

The solitary pupal parasitoid Diadromus pulchellus was released in 2010 as a classical biological control agent against leek moth, Acrolepiopsis assectella, an important new pest of onion crops, Allium spp. in Eastern North America. Post-release monitoring using sentinel leek moth pupae revealed that the facultative hyperparasitoid Conura albifrons was attacking leek moth and potentially D. pulchellus as well. We used laboratory choice and no-choice tests to assess the potential impact of C. albifrons on leek moth and D. pulchellus. C. albifrons is capable of developing in newly formed leek moth pupae and leek moth pupae containing first instar D. pulchellus, as well as in fully developed D. pulchellus pupae. Survivorship of both leek moth and D. pulchellus exposed to C. albifrons was significantly lower than that of unexposed controls. In choice trials, prior host experience significantly influenced host choice by C. albifrons. These results suggest that C. albifrons could impact the establishment of D. pulchellus through both competition and intraguild predation, and that the impact has the potential to change as the relative frequency of the two hosts shifts in field populations.

Testing the habituation assumption underlying models of parasitoid foraging behavior

Background Habituation, a form of non-associative learning, has several well-defined characteristics that apply to a wide range of physiological and behavioral responses in many organisms. In classic patch time allocation models, habituation is considered to be a major mechanistic component of parasitoid behavioral strategies. However, parasitoid behavioral responses to host cues have not previously been tested for the known, specific characteristics of habituation. Methods In the laboratory, we tested whether the foraging behavior of the egg parasitoid Trissolcus basalis shows specific characteristics of habituation in response to consecutive encounters with patches of host (Nezara viridula) chemical contact cues (footprints), in particular: (i) a training interval-dependent decline in response intensity, and (ii) a training interval-dependent recovery of the response. Results As would be expected of a habituated response, wasps trained at higher frequencies decreased their behavioral response to host footprints more quickly and to a greater degree than those trained at low frequencies, and subsequently showed a more rapid, although partial, recovery of their behavioral response to host footprints. This putative habituation learning could not be blocked by cold anesthesia, ingestion of an ATPase inhibitor, or ingestion of a protein synthesis inhibitor. Discussion Our study provides support for the assumption that diminishing responses of parasitoids to chemical indicators of host presence constitutes habituation as opposed to sensory fatigue, and provides a preliminary basis for exploring the underlying mechanisms.