Antipredatory Responses of Mosquito Pupae to Non-Lethal Predation Threat-Behavioral Plasticity Across Life-History Stages.

Antipredatory behavioral responses tend to be energetically expensive, and prey species thus need to resolve trade-offs between these behaviors and other activities such as foraging and mating. While these trade-offs have been well-studied across taxa, less is known about how costs and benefits vary in different life-history contexts, and associated consequences. To address this question, we compared responses of the yellow fever mosquito (Aedes aegypti [Diptera: Culicidae]) to predation threat from guppy (Poecilia reticulata [Cyprinodontiformes: Poeciliidae]) across two life-history stages-larvae (data from previous study) and pupae (from this study). Pupae are motile but do not feed and are comparable to larvae in terms of behavior. To understand how physiological costs affect the threat sensitivity of pupae, we used sex (with size as a covariate) as a proxy for stored energy reserves, and quantified movement and space use patterns of male (small-sized) and female (large-sized) pupae when exposed to predation threat. We found that pupae did not alter movement when exposed to predator cues but instead altered spatial use by spending more time at the bottom of the water column. We found no effect of pupa sex (or size) on the behavioral responses we measured. We conclude that pupa behavior, both antipredatory and otherwise, is primarily targeted at minimizing energy expenditure, as compared with larval behavior, which appears to balance energy expenditure between the opposing pressures of foraging and of avoiding predation. We suggest that antipredatory defenses in metamorphosing prey are modulated by varying energetic trade-offs associated with different life-history stages.

The enemy of my enemy: multiple interacting selection pressures lead to unexpected anti-predator responses.

Despite being a major selective force, predation can induce puzzling variability in anti-predator responses-from lack of predator aversion to lifelong predator-induced fear. This variability is hypothesised to result from variation in the trade-offs associated with avoiding predators. But critical information on fitness outcomes of these trade-offs associated with anti-predator behaviours is lacking. We tested this trade-off hypothesis in Aedes aegypti, by examining oviposition site selection decisions in response towards larval predation risk and comprehensively measuring the fitness implications of trade-offs of avoiding larval predators, using three fitness measures: larval survival, development time and size. In a field study, we find that adult females show a surprisingly variable response to predators, ranging from attraction to avoidance. This variation is explained by fitness outcomes of oviposition along a predation-risk gradient that we measured in the laboratory. We show that ovipositing females could gain fitness benefits from ovipositing in pools with a low density of predators, rather than in predator-free pools, as predators provide a release from negative density effects of conspecific larvae that might co-occur in a pool. Interacting selection pressures may thus explain diverse prey responses. We suggest other systems in which similarly unexpected prey behaviour is likely to occur.

Ants on Clerodendrum infortunatum: Disentangling Effects of Larceny and Herbivory.

Nectar larcenists extract nectar from flowers without pollinating them. A reasonable expectation is that any form of nectar larceny should have a detrimental effect on the plant's reproductive success. However, studies reveal an entire range of effects, from highly negative to highly positive. This variation in effect may be partly explained by additional, unmeasured, effects of nectar larcenists on plants. In a study system where two ant species Tapinoma melanocephalum (Fabr.) (Hymenoptera: Formicidae) and Trichomyrmex destructor (Jerd.) (Hymenoptera: Formicidae) act as nectar larcenists, we examined the effect of larceny on the female reproductive success of Clerodendrum infortunatum Gaertn. (Lamiales: Lamiaceae) in rain forest fragments of the Western Ghats, India. This was done through a combination of field observations and a series of field experiments looking at the effects of excluding ants from inflorescences. We found that T. destructor reduces fruit set considerably. Rather than this being a consequence of nectar larceny, however, our experiments show that the negative effect arises instead from the herbivorous behavior of the ant. At a population level, both ant species prefer edges over interiors of forest patches, spatially concentrating the interaction zone to forest edges. Simultaneously considering multiple ecological interactions and disentangling their relative contributions might explain the large variation across species in the observed effect of larceny. The overall population effect of nectar larceny and herbivory is likely to depend on the spatial structuring of plants and ants.

Context-dependent interactive effects of non-lethal predation on larvae impact adult longevity and body composition.

Predation impacts development, behavior and morphology of prey species thereby shaping their abundances, distribution and community structure. Non-lethal threat of predation, specifically, can have a strong influence on prey lifehistory characteristics. While investigations often focus on the impact of predation threat on prey in isolation, tests of its interactive effects with food availability and resource competition on prey survival and fitness can improve understanding of costs, benefits and trade-offs of anti-predator strategies. This study, involving Aedes aegypti mosquitoes as a model organism, investigates both simple and interactive effects of predation threat during the larval stage on survival, size at and time to maturity, stored teneral reserves of glycogen, protein and lipid in adults, and adult longevity. Our results show that development times of mosquito larvae were increased (by 14.84% in males and by 97.63% in females), and size of eclosing adults decreased (by 62.30% in males and by 58.33% in females) when exposed to lowered nutrition and elevated intraspecific competition, but that predation had no detectable effect on these simple traits. Teneral reserves of glycogen, protein and lipid and adult longevity were positively correlated with adult body size. Non-lethal predation threat had significant interactive effects with nutrition and larval competition on teneral reserves in males and adult longevity in males and females. The sexes responded differently to conditions encountered as larvae, with the larval environment affecting development and adult characteristics more acutely for females than for males. The outcome of this study shows how threat of predation on juveniles can have long-lasting effects on adults that are likely to impact mosquito population dynamics and that may impact disease transmission.

Influence of gaze and directness of approach on the escape responses of the Indian rock lizard, Psammophilus dorsalis (Gray, 1831).

Animals often evaluate the degree of risk posed by a predator and respond accordingly. Since many predators orient their eyes towards prey while attacking, predator gaze and directness of approach could serve as conspicuous indicators of risk to prey. The ability to perceive these cues and discriminate between high and low predation risk should benefit prey species through both higher survival and decreased energy expenditure. We experimentally examined whether Indian rock lizards (Psammophilus dorsalis) can perceive these two indicators of predation risk by measuring the variation in their fleeing behaviour in response to type of gaze and approach by a human predator. Overall, we found that the gaze and approach of the predator influenced flight initiation distance, which also varied with attributes of the prey (i.e. size/sex and tail-raise behaviour). Flight initiation distance (FID) was 43 percent longer during direct approaches with direct gaze compared with tangential approaches with averted gaze. In further, exploratory, analyses, we found that FID was 23 percent shorter for adult male lizards than for female or young male (FYM) lizards. In addition, FYM lizards that showed a tail-raise display during approach had a 71 percent longer FID than those that did not. Our results suggest that multiple factors influence the decision to flee in animals. Further studies are needed to test the generality of these factors and to investigate the proximate mechanisms underlying flight decisions.

To eat and not be eaten: modelling resources and safety in multi-species animal groups.

Using mixed-species bird flocks as an example, we model the payoffs for two types of species from participating in multi-species animal groups. Salliers feed on mobile prey, are good sentinels and do not affect prey capture rates of gleaners; gleaners feed on prey on substrates and can enhance the prey capture rate of salliers by flushing prey, but are poor sentinels. These functional types are known from various animal taxa that form multi-species associations. We model costs and benefits of joining groups for a wide range of group compositions under varying abundances of two types of prey-prey on substrates and mobile prey. Our model predicts that gleaners and salliers show a conflict of interest in multi-species groups, because gleaners benefit from increasing numbers of salliers in the group, whereas salliers benefit from increasing gleaner numbers. The model also predicts that the limits to size and variability in composition of multi-species groups are driven by the relative abundance of different types of prey, independent of predation pressure. Our model emphasises resources as a primary driver of temporal and spatial group dynamics, rather than reproductive activity or predation per se, which have hitherto been thought to explain patterns of multi-species group formation and cohesion. The qualitative predictions of the model are supported by empirical patterns from both terrestrial and marine multi-species groups, suggesting that similar mechanisms might underlie group dynamics in a range of taxa. The model also makes novel predictions about group dynamics that can be tested using variation across space and time.

Protecting important sites for biodiversity contributes to meeting global conservation targets.

Protected areas (PAs) are a cornerstone of conservation efforts and now cover nearly 13% of the world's land surface, with the world's governments committed to expand this to 17%. However, as biodiversity continues to decline, the effectiveness of PAs in reducing the extinction risk of species remains largely untested. We analyzed PA coverage and trends in species' extinction risk at globally significant sites for conserving birds (10,993 Important Bird Areas, IBAs) and highly threatened vertebrates and conifers (588 Alliance for Zero Extinction sites, AZEs) (referred to collectively hereafter as 'important sites'). Species occurring in important sites with greater PA coverage experienced smaller increases in extinction risk over recent decades: the increase was half as large for bird species with>50% of the IBAs at which they occur completely covered by PAs, and a third lower for birds, mammals and amphibians restricted to protected AZEs (compared with unprotected or partially protected sites). Globally, half of the important sites for biodiversity conservation remain unprotected (49% of IBAs, 51% of AZEs). While PA coverage of important sites has increased over time, the proportion of PA area covering important sites, as opposed to less important land, has declined (by 0.45-1.14% annually since 1950 for IBAs and 0.79-1.49% annually for AZEs). Thus, while appropriately located PAs may slow the rate at which species are driven towards extinction, recent PA network expansion has under-represented important sites. We conclude that better targeted expansion of PA networks would help to improve biodiversity trends.

Ancient host specificity within a single species of brood parasitic bird.

Parasites that exploit multiple hosts often experience diversifying selection for host-specific adaptations. This can result in multiple strains of host specialists coexisting within a single parasitic species. A long-standing conundrum is how such sympatric host races can be maintained within a single parasitic species in the face of interbreeding among conspecifics specializing on different hosts. Striking examples are seen in certain avian brood parasites such as cuckoos, many of which show host-specific differentiation in traits such as host egg mimicry. Exploiting a Zambian egg collection amassed over several decades and supplemented by recent fieldwork, we show that the brood parasitic Greater Honeyguide Indicator indicator exhibits host-specific differentiation in both egg size and egg shape. Genetic analysis of honeyguide eggs and chicks show that two highly divergent mitochondrial DNA lineages are associated with ground- and tree-nesting hosts, respectively, indicating perfect fidelity to two mutually exclusive sets of host species for millions of years. Despite their age and apparent adaptive diversification, however, these ancient lineages are not cryptic species; a complete lack of differentiation in nuclear genes shows that mating between individuals reared by different hosts is sufficiently frequent to prevent speciation. These results indicate that host specificity is maternally inherited, that host-specific adaptation among conspecifics can be maintained without reproductive isolation, and that host specificity can be remarkably ancient in evolutionary terms.

The impact of conservation on the status of the world's vertebrates.

Using data for 25,780 species categorized on the International Union for Conservation of Nature Red List, we present an assessment of the status of the world's vertebrates. One-fifth of species are classified as Threatened, and we show that this figure is increasing: On average, 52 species of mammals, birds, and amphibians move one category closer to extinction each year. However, this overall pattern conceals the impact of conservation successes, and we show that the rate of deterioration would have been at least one-fifth again as much in the absence of these. Nonetheless, current conservation efforts remain insufficient to offset the main drivers of biodiversity loss in these groups: agricultural expansion, logging, overexploitation, and invasive alien species.

The nuclear question: rethinking species importance in multi-species animal groups.

1. Animals group for various benefits, and may form either simple single-species groups, or more complex multi-species associations. Multi-species groups are thought to provide anti-predator and foraging benefits to participant individuals. 2. Despite detailed studies on multi-species animal groups, the importance of species in group initiation and maintenance is still rated qualitatively as 'nuclear' (maintaining groups) or 'attendant' (species following nuclear species) based on species-specific traits. This overly simplifies and limits understanding of inherently complex associations, and is biologically unrealistic, because species roles in multi-species groups are: (i) likely to be context-specific and not simply a fixed species property, and (ii) much more variable than this dichotomy indicates. 3. We propose a new view of species importance (measured as number of inter-species associations), along a continuum from 'most nuclear' to 'least nuclear'. Using mixed-species bird flocks from a tropical rainforest in India as an example, we derive inter-species association measures from randomizations on bird species abundance data (which takes into account species 'availability') and data on 86 mixed-species flocks from two different flock types. Our results show that the number and average strength of inter-species associations covary positively, and we argue that species with many, strong associations are the most nuclear. 4. From our data, group size and foraging method are ecological and behavioural traits of species that best explain nuclearity in mixed-species bird flocks. Parallels have been observed in multi-species fish shoals, in which group size and foraging method, as well as diet, have been shown to correlate with nuclearity. Further, the context in which multi-species groups occur, in conjunction with species-specific traits, influences the role played by a species in a multi-species group, and this highlights the importance of extrinsic factors in shaping species importance. 5. Our view of nuclearity provides predictive power in examining species roles in a variety of situations (e.g. predicting leadership in differently composed communities), and can be applied to examine a broad range of ecological and evolutionary questions pertinent to multi-species groups in general.

Global biodiversity: indicators of recent declines.

In 2002, world leaders committed, through the Convention on Biological Diversity, to achieve a significant reduction in the rate of biodiversity loss by 2010. We compiled 31 indicators to report on progress toward this target. Most indicators of the state of biodiversity (covering species' population trends, extinction risk, habitat extent and condition, and community composition) showed declines, with no significant recent reductions in rate, whereas indicators of pressures on biodiversity (including resource consumption, invasive alien species, nitrogen pollution, overexploitation, and climate change impacts) showed increases. Despite some local successes and increasing responses (including extent and biodiversity coverage of protected areas, sustainable forest management, policy responses to invasive alien species, and biodiversity-related aid), the rate of biodiversity loss does not appear to be slowing.

Improvements to the Red List Index.

The Red List Index uses information from the IUCN Red List to track trends in the projected overall extinction risk of sets of species. It has been widely recognised as an important component of the suite of indicators needed to measure progress towards the international target of significantly reducing the rate of biodiversity loss by 2010. However, further application of the RLI (to non-avian taxa in particular) has revealed some shortcomings in the original formula and approach: It performs inappropriately when a value of zero is reached; RLI values are affected by the frequency of assessments; and newly evaluated species may introduce bias. Here we propose a revision to the formula, and recommend how it should be applied in order to overcome these shortcomings. Two additional advantages of the revisions are that assessment errors are not propagated through time, and the overall level extinction risk can be determined as well as trends in this over time.

Mother guarding: how offspring may influence the extra-pair behaviour of their parents.

In this paper we propose a novel form of social control of mate choice. Through mother guarding, offspring can help in protecting the paternity of their father by preventing their mother from engaging in extra-pair matings. We present a model that predicts the circumstances under which mothers should be selected to seek or avoid extra-pair matings, and existing offspring should be selected to prevent or promote such matings. In its simplest form, our model shows that offspring are selected to mother guard as long as the viability of extra-pair young is less than twice that of within-pair young; when the relative viability is greater, offspring are selected to promote extra-pair mating by their mother. If the existing offspring are not necessarily sired by their mother's social mate, then the potential for conflict is further reduced. We also consider whether offspring have an interest in the extra-pair reproduction of their fathers. We show that when the costs of the father's infidelity to the mother's brood are high, existing offspring are selected to prevent extra-pair mating by their father; when such costs are low, offspring are selected to promote extra-pair mating by their father. In principle, our model applies to all species where offspring show delayed dispersal and where breeding pairs raise multiple broods or litters. This situation exists in, but is not limited to, the majority of cooperatively breeding species. The significance of this model with regard to our current understanding of the evolution of extra-pair behaviour in such species is discussed.