Hawksbill sea turtle Eretmochelys imbricata nesting on Long Island, Antigua, West Indies (also known as Jumby Bay) has been monitored since 1987. Although the numbers of nesting females remained relatively constant for the first 11 survey seasons (1987)(1988)(1989)(1990)(1991)(1992)(1993)(1994)(1995)(1996)(1997), inclusion of more recent data (1998)(1999)(2000)(2001)(2002)(2003)(2004) in the analysis reveals a statistically significant upward trend. In particular, neophytes have shown a significant upturn in numbers, whereas the remigrant subpopulation has remained stationary. This indicates that recruitment is driving the upward trend in the total number of nesters. Predictive models based on the Poisson distribution suggest that the neophyte subpopulation will continue to grow in size by an average of 10% per annum. Model-based predictions and their limitations are discussed. The Jumby Bay Hawksbill Project, which has monitored and protected nesting hawksbills and their eggs since the project's onset, is one among several factors that may contribute to the recent increase in nesting females.
Defense against natural enemies constitutes an important driver of herbivore host range evolution in the wild. Populations of the Baltimore checkerspot butterfly, Euphydryas phaeton (Nymphalidae), have recently incorporated an exotic plant, Plantago lanceolata (Plantaginaceae), into their dietary range. To understand the tritrophic consequences of utilizing this exotic host plant, we examined immune performance, chemical defense, and interactions with a natural entomopathogen (Junonia coenia densovirus, Parvoviridae) across wild populations of this specialist herbivore. We measured three immune parameters, sequestration of defensive iridoid glycosides (IGs), and viral infection load in field‐collected caterpillars using either P. lanceolata or a native plant, Chelone glabra (Plantaginaceae). We found that larvae using the exotic plant exhibited reduced immunocompetence, compositional differences in IG sequestration, and higher in situ viral burdens compared to those using the native plant. On both host plants, high IG sequestration was associated with reduced hemocyte concentration in the larval hemolymph, providing the first evidence of incompatibility between sequestered chemical defenses and the immune response (i.e., the “vulnerable host” hypothesis) from a field‐based study. However, despite this negative relationship between IG sequestration and cellular immunity, caterpillars with greater sequestration harbored lower viral loads. While survival of virus‐infected individuals decreased with increasing viral burden, it ultimately did not differ between the exotic and native plants. These results provide evidence that: (1) phytochemical sequestration may contribute to defense against pathogens even when immunity is compromised and (2) herbivore persistence on exotic plant species may be facilitated by sequestration and its role in defense against natural enemies.
A rapidly advancing area of ecological immunology concerns the effects of diet on animals' immunological responses to parasites and pathogens. Here, we focus on diet-mediated ecological immunology in herbivorous insects, in part because these organisms commonly experience nutritional limitations from their diets of plants. Nutritional immunology highlights nutrient-based trade-offs between immunological and other physiological processes as well as trade-offs among distinct immunological processes. This field reveals that nutrition influences the quality and quantity of immunological defense in herbivorous insects, and conversely that nutritional intake by herbivorous insects can be an adaptive response to the specific types of immune-challenge they face in the context of other physiological processes. Because the diets of herbivores challenge them physiologically with plants' secondary metabolites, another area of study analyzes constraints on immunological defense imposed by secondary metabolites of plants in the diets of herbivorous insects. Alternatively, some herbivores can use secondary metabolites as medicine against parasites or pathogens. Animal-medication theory makes an important contribution to ecological immunology by distinguishing prophylactic and therapeutic mechanisms of anti-parasite defense. Integrating ideas from animal-medication and nutritional immunology, we outline a conceptual framework in which the immunological role of the diet consists of mechanisms of prophylaxis, therapy, compensation, and combinations thereof. Then, we use this framework to organize findings from our own research on diet-mediated ecological immunology of woolly bear caterpillars. We show evidence that the woolly bear caterpillar, Grammia incorrupta (Hy. Edwards) (Lepidoptera, Erebidae, and Arctiinae), can employ both diet-mediated prophylaxis and therapy. First, increased consumption of carbohydrate-biased food prior to immune-challenge increased its melanization-response. Second, increased consumption of pyrrolizidine alkaloids (PAs) more than 24 h after parasitism by tachinid flies resulted in anti-parasite resistance. Caterpillars reduced feeding on protein-biased food within 24 h after immune-challenge, showing evidence of illness-induced anorexia. We synthesize our work to generate the hypothesis that a diet-mediated defense by the host against parasites acts as a temporally explicit, multi-stage process.
This study investigates complex effects of parasitoid infection on herbivore diet choice. Specifically, we examine how immunological resistance, parasitoid infection stage, and parasitoid taxonomic identity affect the pharmacophagous behavior of the polyphagous caterpillar, Grammia incorrupta (Arctiidae). Using a combination of lab and field experiments, we test the caterpillar's pharmacophagous response to pyrrolizidine alkaloids (PAs) over the course of parasitoid infection, as well as the effect of dietary PAs on the caterpillar's immunological response. Previous work from other systems gave the prediction that dietary PAs would be detrimental to the immune response and thus less acceptable to feeding early in the infection, when encapsulation of the parasitoid is most crucial. We found that the feeding acceptability of PAs was indeed low for caterpillars with early-stage parasitoid infections; however, this was not explained by PA interference with immune function. When allowed to choose among three host plant species, individuals harboring early-stage parasitoids increased their consumption of a nutritious plant containing antioxidants. This result was driven by wasp-parasitized caterpillars, whereas fly-parasitized caterpillars increased their consumption of plants containing iridoid glycosides. Individuals in the later time phase of infection exhibited an increase in PA intake that was consistent with previously reported self-medication behavior during late-stage parasitoid infection. This study reveals the depth of complexity and the dynamic nature of herbivore host plant choice, and underscores the importance of considering multitrophic interactions when studying insect diet choice.
Understanding population dynamics, and how it is influenced by exogenous and endogenous factors, is important to the study and conservation of species. Moreover, for migratory species, the phenology and duration of use of a given location can also influence population structure and dynamics. For many species, breeding abundance, survival, and reproductive performance, as well as phenology of nesting, are often the most accessible, and therefore, practical elements of their life history to study. For a population of hawksbill sea turtles (Eretmochelys imbricata), we modeled population change for nesters and total adult females, survival, and breeding probability, from 25 yr of intensive tagging data. We modeled breeding probability as a function of the number of years since last breeding and tested for differences between neophyte and experienced nesters. For each year, we also estimated the number of clutches deposited per female, and phenology of use, for neophytes and experienced nesters. To implement the analysis, we developed a novel generalized multistate open robust design mark–recapture modeling framework, with parameters for survival and transition probabilities, and for each primary period, state structure and arrival, persistence, and detection probabilities. Derived parameters included abundance of observable and unobservable components of the population, residence time, expected arrival and departure periods, and per‐period intensity of study area use. Abundance of nesters increased over most of the time series. Survival probability was 0.935 ± 0.01 (estimate ± SE). Virtually all hawksbills skipped at least one year of nesting. Breeding probability increased by skipping a second year, but then decreased thereafter. Subsequent breeding probability was lower for neophyte nesters than for experienced nesters, but the effect was weaker than the effect of years since breeding. Clutch frequency varied by year, with no discernable pattern of differences between neophytes and experienced nesters. Mean arrival and departure dates also varied, with a slight shift of nesting activity to earlier in the season. The multistate open robust design model developed here provides a flexible framework for modeling the dynamics of structured migratory populations and the phenology and duration of their seasonal use of study areas.
Factors including host abundance, quality, and the degree to which hosts provide enemy‐free space (EFS) may drive host plant choice by phytophagous insects. Herbivores may also experience fitness tradeoffs among hosts, promoting polyphagy. The fall webworm Hyphantria cunea is a dietary generalist that feeds on a broad array of trees across its geographic range. Here, we investigate the drivers of host tree use by the fall webworm in Connecticut (CT) and Maryland (MD). Neither caterpillar performance nor EFS was associated with the frequency with which host trees were used, and no tradeoff between host quality and EFS was identified. Vegetation surveys adjacent to host trees showed that at both localities, host use was non‐random with respect to tree species, and that the main predictor of use among suitable host trees was host tree abundance. This suggests that webworms are under selection to reduce search time for oviposition sites. Although we did not detect a tradeoff between host plant quality and availability in MD, we did identify that tradeoff in CT. This disparity amid otherwise similar patterns of host use between CT and MD may be explained by the relative rarity of high quality hosts in CT compared to MD. Our results illustrate that geographic mosaics in patterns of host use may arise in the absence of local adaptation if host use is based upon availability rather than host plant attributes.
Summary The myriad chemicals produced by plants may act in combination to enhance chemical defence against herbivores. Many animals have evolved the ability to harness plant secondary metabolites (PSMs) and other chemical resources for their own defence, but few studies have addressed the compelling notion that non‐human animals combine exogenous chemicals from different sources to defend themselves against predators, parasites and pathogens. We consider the use of ‘defensive cocktails’ from an evolutionary ecology perspective, introducing the term, ‘acquired combinatorial chemical defence’ (ACCD). We define ACCD as the adaptive use of multiple chemicals of discrete origin resulting in defence against natural enemies. First, we discuss the defining characteristics of ACCD: the ability to harness interspecific chemical variation, to independently regulate it, and to obtain defensive benefits via synergy that exceed those associated with single sources. Then, we describe three non‐mutually exclusive modes by which acquired chemicals may operate against natural enemies: different chemical resources may provide defence during different stages of development, may be effective against different enemies or may work additively or synergistically against a given enemy at a given developmental stage. Next, we describe possible avenues by which chemical combinations may be acquired by herbivores and other taxa, including the mixing of exogenous chemicals from different items in the diet and mixing chemicals of dietary origin with those from non‐food resources. We discuss possible costs of ACCD, including detoxification costs and interactions with the immune system, and discuss methods of testing for ACCD and its costs. Finally, we discuss the evolutionary prediction that herbivores may converge on the use of complementary combinations of chemical resources from the environment or chemical defence syndromes. Opportunities to combine chemical resources abound, suggesting that animal and human medication may be more closely aligned than previously recognized.
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