Ant-plant mutualism: a dietary by-product of a tropical ant's macronutrient requirements.

Many arboreal ants depend on myrmecophytic plants for both food and shelter; in return, these ants defend their host plants against herbivores, which are often insects. Ant-plant and other mutualisms do not necessarily involve the exchange of costly rewards or services; they may instead result from by-product benefits, or positive outcomes that do not entail a cost for one or both partners. Here, we examined whether the plant-ant Allomerus octoarticulatus pays a short-term cost to defend their host plants against herbivores, or whether plant defense is a by-product benefit of ant foraging for insect prey. Because the food offered by ant-plants is usually nitrogen-poor, arboreal ants may balance their diets by consuming insect prey or associating with microbial symbionts to acquire nitrogen, potentially shifting the costs and benefits of plant defense for the ant partner. To determine the effect of ant diet on an ant-plant mutualism, we compared the behavior, morphology, fitness, stable isotope signatures, and gaster microbiomes of A. octoarticulatus ants nesting in Cordia nodosa trees maintained for nearly a year with or without insect herbivores. At the end of the experiment, ants from herbivore exclosures preferred protein-rich baits more than ants in the control (i.e., herbivores present) treatment. Furthermore, workers in the control treatment were heavier than in the herbivore-exclusion treatment, and worker mass predicted reproductive output, suggesting that foraging for insect prey directly increased ant colony fitness. The gaster microbiome of ants was not significantly affected by the herbivore exclusion treatment. We conclude that the defensive behavior of some phytoecious ants is a by-product of their need for external protein sources; thus, the consumption of insect herbivores by ants benefits both the ant colony and the host plant.

The direct and ecological costs of an ant-plant symbiosis.

How strong is selection for cheating in mutualisms? The answer depends on the type and magnitude of the costs of the mutualism. Here we investigated the direct and ecological costs of plant defense by ants in the association between Cordia nodosa, a myrmecophytic plant, and Allomerus octoarticulatus, a phytoecious ant. Cordia nodosa trees produce food and housing to reward ants that protect them against herbivores. For nearly 1 year, we manipulated the presence of A. octoarticulatus ants and most insect herbivores on C. nodosa in a full-factorial experiment. Ants increased plant growth when herbivores were present but decreased plant growth when herbivores were absent, indicating that hosting ants can be costly to plants. However, we did not detect a cost to ant colonies of defending host plants against herbivores. Although this asymmetry in costs suggests that the plants may be under stronger selection than the ants to cheat by withholding investment in their partner, the costs to C. nodosa are probably at least partly ecological, arising because ants tend scale insects on their host plants. We argue that ecological costs should favor resistance or traits other than cheating and thus that neither partner may face much temptation to cheat.

Nutritional state and collective motion: from individuals to mass migration.

In order to move effectively in unpredictable or heterogeneous environments animals must make appropriate decisions in response to internal and external cues. Identifying the link between these components remains a challenge for movement ecology and is important in understanding the mechanisms driving both individual and collective motion. One accessible way of examining how internal state influences an individual's motion is to consider the nutritional state of an animal. Our experimental results reveal that nutritional state exerts a relatively minor influence on the motion of isolated individuals, but large group-level differences emerge from diet affecting inter-individual interactions. This supports the idea that mass movement in locusts may be driven by cannibalism. To estimate how these findings are likely to impact collective migration of locust hopper bands, we create an experimentally parametrized model of locust interactions and motion. Our model supports our hypothesis that nutrient-dependent social interactions can lead to the collective motion seen in our experiments and predicts a transition in the mean speed and the degree of coordination of bands with increasing insect density. Furthermore, increasing the interaction strength (representing greater protein deprivation) dramatically reduces the critical density at which this transition occurs, demonstrating that individuals' nutritional state could have a major impact on large-scale migration.

Speed over efficiency: locusts select body temperatures that favour growth rate over efficient nutrient utilization.

Ectotherms have evolved preferences for particular body temperatures, but the nutritional and life-history consequences of such temperature preferences are not well understood. We measured thermal preferences in Locusta migratoria (migratory locusts) and used a multi-factorial experimental design to investigate relationships between growth/development and macronutrient utilization (conversion of ingesta to body mass) as a function of temperature. A range of macronutrient intake values for insects at 26, 32 and 38 degrees C was achieved by offering individuals high-protein diets, high-carbohydrate diets or a choice between both. Locusts placed in a thermal gradient selected temperatures near 38 degrees C, maximizing rates of weight gain; however, this enhanced growth rate came at the cost of poor protein and carbohydrate utilization. Protein and carbohydrate were equally digested across temperature treatments, but once digested both macronutrients were converted to growth most efficiently at the intermediate temperature (32 degrees C). Body temperature preference thus yielded maximal growth rates at the expense of efficient nutrient utilization.

Crowded locusts produce hatchlings vulnerable to fungal attack.

Transgenerational effects of parental experience on offspring immunity are well documented in the vertebrate literature (where antibodies play an obligatory role), but have only recently been described in invertebrates. We have assessed the impact of parental rearing density upon offspring disease resistance by challenging day-old locust hatchlings (Schistocerca gregaria) from either crowd- or solitary-reared parents with the fungal pathogen Metarhizium anisopliae var. acridum. When immersed in standardized conidia suspensions, hatchlings from gregarious parents suffered greater pathogen-induced mortality than hatchlings from solitary-reared parents. This observation contradicts the basic theory of positive density-dependent prophylaxis and demonstrates that crowding has a transgenerational influence upon locust disease resistance.

Maternal effects on phase characteristics in the desert locust, Schistocerca gregaria: a review of current understanding.

Desert locusts demonstrate pronounced density-dependent polyphenism: a complex suite of traits shifts over the lifetime of an individual in response to crowding or isolation. These changes also accumulate across generations through a maternal effect. Female desert locusts alter the developmental trajectory of their offspring in response to their own experience of crowding. The mother possesses a memory of both the recency and extent of crowding and shifts the phase state of her hatchlings accordingly. Extensive experimental work has shown that offspring behaviour is controlled by a low molecular weight, polar compound (or compounds) released from the mother's accessory glands. The chemical identity of this agent is not yet known.

Neural correlates of competing fear behaviors evoked by an innately aversive stimulus.

Environment and experience influence defensive behaviors, but the neural circuits mediating such effects are not well understood. We describe a new experimental model in which either flight or freezing reactions can be elicited from mice by innately aversive ultrasound. Flight and freezing are negatively correlated, suggesting a competition between fear motor systems. An unfamiliar environment or a previous aversive event, moreover, can alter the balance between these behaviors. To identify potential circuits controlling this competition, global activity patterns in the whole brain were surveyed in an unbiased manner by c-fos in situ hybridization, using novel experimental and analytical methods. Mice predominantly displaying freezing behavior had preferential neural activity in the lateral septum ventral and several medial and periventricular hypothalamic nuclei, whereas mice predominantly displaying flight had more activity in cortical, amygdalar, and striatal motor areas, the dorsolateral posterior zone of the hypothalamus, and the vertical limb of the diagonal band. These complementary patterns of c-fos induction, taken together with known connections between these structures, suggest ways in which the brain may mediate the balance between these opponent defensive behaviors.

Swarm formation in the desert locust Schistocerca gregaria: isolation and NMR analysis of the primary maternal gregarizing agent.

Depending on their rearing density, female desert locusts Schistocerca gregaria epigenetically endow their offspring with differing phenotypes. To identify the chemical basis for such maternal transmission, we compared solitarious and gregarious locust egg pod foam using high performance liquid chromatography (HPLC). We revealed causal relationships between foam chemistry and hatchling phenotype (phase state) by iteratively applying HPLC fractions from gregarious locust egg foam extracts to solitarious eggs and assessing resulting hatchlings with a behavioural bioassay involving logistic regression. Selection and application of increasingly specific HPLC fractions allowed us to isolate compounds with gregarizing properties. Hatchling gregarization was triggered only by certain fractions and was dose dependent. In a final series of experiments, we characterized the most specific gregarizing fraction by nuclear magnetic resonance (NMR) spectroscopy. Here we present tentative structural features of the primary locust maternal gregarizing agent, which appears to be an alkylated l-dopa analogue. In addition, we propose a mechanism for phase-dependent regulation of this compound's activity.