Dropping to escape: a review of an under‐appreciated antipredator defence

Dropping is a common antipredator defence that enables rapid escape from a perceived threat. However, despite its immediate effectiveness in predator–prey encounters (and against other dangers such as a parasitoid or an aggressive conspecific), it remains an under‐appreciated defence strategy in the scientific literature. Dropping has been recorded in a wide range of taxa, from primates to lizards, but has been studied most commonly in insects. Insects have been found to utilise dropping in response to both biotic and abiotic stimuli, sometimes dependent on mechanical or chemical cues. Whatever the trigger for dropping, the decision to drop by prey will present a range of inter‐related costs and benefits to the individual and so there will be subtle complexities in the trade‐offs surrounding this defensive behaviour. In predatory encounters, dropping by prey will also impose varying costs and benefits on the predator – or predators – involved in the system. There may be important trade‐offs involved in the decision made by predators regarding whether to pursue prey or not, but the predator perspective on dropping has been less explored at present. Beyond its function as an escape tactic, dropping has also been suggested to be an important precursor to flight in insects and further study could greatly improve understanding of its evolutionary importance. Dropping in insects could also prove of significant practical importance if an improved understanding can be applied to integrated pest‐management strategies. Currently the non‐consumptive effects of predators on their prey are under‐appreciated in biological control and it may be that the dropping behaviour of many pest species could be exploited via management practices to improve crop protection. Overall, this review aims to provide a comprehensive synthesis of the current literature on dropping and to raise awareness of this fascinating and widespread behaviour. It also seeks to offer some novel hypotheses and highlight key avenues for future research.     

Dropping behaviour of larvae of aphidophagous ladybirds and its effects on incidence of intraguild predation: interactions between the intraguild prey, Adalia bipunctata (L.) and Coccinella septempunctata (L.), and the intraguild predator, Harmonia axyridis Pallas

Abstract.  1. Two experiments were performed in the laboratory to assess the behaviour of dropping from a host plant as a defence against intraguild predation in aphidophagous ladybird larvae.
2. In the first experiment, encounters were observed on bean plants between fourth instars of the intraguild predator species, Harmonia axyridis , and first instars of two other ladybird species, Adalia bipunctata (L.) and Coccinella septempunctata (L.). The percentages of first instars of the latter two species that dropped from the plant in response to attack differed dramatically, with 47.5% of C. septempunctata first instars dropping vs. 0% of A. bipunctata .
3. In the second experiment, first instars of A. bipunctata or C. septempunctata and a fourth instar of H. axyridis were allowed to forage together on bean plants for 3 h. During this time, 44.3% of C. septempunctata larvae dropped from the plant, but less than 2% of A. bipunctata larvae did so. In contrast, 95.0% of A. bipunctata larvae fell victim to intraguild predation by H. axyridis vs. only 54.5% of C. septempunctata larvae.
4. The significance of dropping behaviour of ladybird larvae as a defence against intraguild predation, and the relationship of dropping behaviour to species-specific habitat affinity of ladybirds, is discussed.     

Mechanisms of plant resistance to viruses

Plants have evolved in an environment rich with microorganisms that are eager to capitalize on the plants' biosynthetic and energy-producing capabilities. There are approximately 450 species of plant-pathogenic viruses, which cause a range of diseases. However, plants have not been passive in the face of these assaults, but have developed elaborate and effective defence mechanisms to prevent, or limit, damage owing to viral infection. Plant resistance genes confer resistance to various pathogens, including viruses. The defence response that is initiated after detection of a specific virus is stereotypical, and the cellular and physiological features associated with it have been well characterized. Recently, RNA silencing has gained prominence as an important cellular pathway for defence against foreign nucleic acids, including viruses. These pathways function in concert to result in effective protection against virus infection in plants.     

Trade‐offs between constitutive and induced defences drive geographical and climatic clines in pine chemical defences

There is increasing evidence that geographic and climatic clines drive the patterns of plant defence allocation and defensive strategies. We quantified early growth rate and both constitutive and inducible chemical defences of 18 Pinaceae species in a common greenhouse environment and assessed their defensive allocation with respect to each species' range across climatic gradients spanning 31^o latitude and 2300 m elevation. Constitutive defences traded‐off with induced defences, and these defensive strategies were associated with growth rate such that slow‐growing species invested more in constitutive defence, whereas fast‐growing species invested more in inducible defence. The position of each pine species along this trade‐off axis was in turn associated with geography; moving poleward and to higher elevations, growth rate and inducible defences decreased, while constitutive defence increased. These geographic patterns in plant defence were most strongly associated with variation in temperature. Climatic and geographical clines thus act as drivers of defence profiles by mediating the constraints imposed by trade‐offs, and this dynamic underlays global patterns of defence allocation.     

Aggregation, defence and warning signals: the evolutionary relationship

In a seminal contribution, Fisher argued how distastefulness could incrementally evolve in a prey species that was distributed in family groups. Many defended prey species occur in aggregations, but did aggregation facilitate the evolution of defence as Fisher proposed or did the possession of a defence allow individuals to enjoy the benefits of group living? Contemporary theory suggests that it can work both ways: pre-existing defences can make the evolution of gregariousness easier, but gregariousness can also aid the evolution of defence and warning signals. Unfortunately, the key phylogenetic analyses to elucidate the ordering of events have been hampered by the relative rarity of gregarious species, which in itself indicates that aggregation is not a pre-requisite for defence. Like the underlying theory, experimental studies have not given a definitive answer to the relative timing of the evolution of defence and aggregation, except to demonstrate that both orderings are possible. Conspicuous signals are unlikely to have evolved in the absence of a defence and aggregated undefended prey are likely to be vulnerable to predation in the absence of satiation effects. It therefore seems most likely that defence generally preceded the evolution of both aggregation and signalling, but alternative routes may well be possible.     

How can automimicry persist when predators can preferentially consume undefended mimics?

It is common for species that possess toxins or other defences to advertise these defences to potential predators using aposematic ("warning") signals. There is increasing evidence that within such species, there are individuals that have reduced or non-existent levels of defence but still signal. This phenomenon (generally called automimicry) has been a challenge to evolutionary biologists because of the need to explain why undefended automimics do not gain such as a fitness advantage by saving the physiological costs of defence that they increase in prevalence within the population, hence making the aposematic signal unreliable. The leading theory is that aposematic signals do not stop all predatory attacks but rather encourage predators to attack cautiously until they have identified the defence level of a specific individual. They can then reject defended individuals and consume the undefended. This theory has recently received strong empirical support, demonstrating that high-accuracy discrimination appears possible. However, this raises a new evolutionary problem: if predators can perfectly discriminate the defended from the undefended and preferentially consume the latter, then how can automimicry persist? Here, we present four different mechanisms that can allow non-trivial levels of automimics to be retained within a population, even in the extreme case where predators can differentiate defended from undefended individuals with 100% accuracy. These involve opportunity costs to the predator of sampling carefully, temporal fluctuation in predation pressure, predation pressure being correlated with the prevalence of automimicry, or developmental or evolutionary constraints on the availability of defence. These mechanisms generate predictions as to the conditions where we would expect aposematically signalling populations to feature automimicry and those where we would not.     

Strong invaders are strong defenders – implications for the resistance of invaded communities

Many ecosystems receive a steady stream of non‐native species. How biotic resistance develops over time in these ecosystems will depend on how established invaders contribute to subsequent resistance. If invasion success and defence capacity (i.e. contribution to resistance) are correlated, then community resistance should increase as species accumulate. If successful invaders also cause most impact (through replacing native species with low defence capacity) then the effect will be even stronger. If successful invaders instead have weak defence capacity or even facilitative attributes, then resistance should decrease with time, as proposed by the invasional meltdown hypothesis. We analysed 1157 introductions of freshwater fish in Swedish lakes and found that species’ invasion success was positively correlated with their defence capacity and impact, suggesting that these communities will develop stronger resistance over time. These insights can be used to identify scenarios where invading species are expected to cause large impact.     

Tasting the difference: do multiple defence chemicals interact in Müllerian mimicry?

Müllerian mimicry, where two unpalatable species share a warning pattern, is classically believed to be a form of mutualism, where the species involved share the cost of predator education. The evolutionary dynamics of Müllerian mimicry have recently become a controversial subject, after mathematical models have shown that if minor alterations are made to assumptions about the way in which predators learn and forget about unpalatable prey, this textbook case of mutualism may not be mutualistic at all. An underlying assumption of these models is that Müllerian mimics possess the same defence chemical. However, some Müllerian mimics are known to possess different defence chemicals. Using domestic chicks as predators and coloured crumbs flavoured with either the same or different unpalatable chemicals as prey, we provide evidence that two defence chemicals can interact to enhance predator learning and memory. This indicates that Müllerian mimics that possess different defence chemicals are better protected than those that share a single defence chemical. These data provide insight into how multiple defence chemicals are perceived by birds,and how they influence the way birds learn and remember warningly coloured prey. They highlight the importance of considering how different toxins in mimicry rings can interact in the evolution and maintenance of Müllerian mimicry and could help to explain the remarkable variation in chemical defences found within and between species.     

Growth and reproductive costs of larval defence in the aposematic lepidopteran Pieris brassicae

1.?Utilization of plant secondary compounds for antipredator defence is common in immature herbivorous insects. Such defences may incur a cost to the animal, either in terms of survival, growth rate or in the reproductive success. 2.?A common defence in lepidopterans is the regurgitation of semi-digested material containing the defensive compounds of the food plant, a defence which has led to gut specialization in this order. Regurgitation is often swift in response to cuticular stimulation and deters predators from consuming or parasitizing the larva. The loss of food and other gut material seems likely to impact on fitness, but evidence is lacking. 3.?Here, we raised larvae of the common crop pest Pieris brassicae on commercial cabbage leaves, simulated predator attacks throughout the larval period, and measured life-history responses. 4.?We found that the probability of survival to pupation decreased with increasing frequency of attacks, but this was because of regurgitation rather than the stimulation itself. There was a growth cost to the defence such that the more regurgitant that individuals produced over the growth period, the smaller they were at pupation. 5.?The number of mature eggs in adult females was positively related to pupal mass, but this relationship was only found when individuals were not subjected to a high frequency of predator simulation. This suggests that there might be cryptic fitness costs to common defensive responses that are paid despite apparent growth rate being maintained. 6.?Our results demonstrate a clear life-history cost of an antipredator defence in a model pest species and show that under certain conditions, such as high predation threat, the expected relationship between female body size and potential fecundity can be disrupted.     

Context-dependent defence in terrestrial plants: the effects of light and nutrient availability on plant resistance against herbivory

The context‐dependent defence (CDD) hypothesis predicts that defence levels of plant species against herbivory are not fixed but vary with environmental conditions, in a way that is specific for plant species that share evolutionary adaptations to resource conditions exemplified by similar maximum relative growth rates. More specifically, we expected plants from resource‐poor environments to display high defence levels but not when grown under resource‐rich conditions, whereas the reverse – plants from resource‐rich conditions displaying low defence levels but not when grown under resource‐poor conditions – is not necessarily the case. In this study, we used multiple‐choice bioassays in which leaf discs were fed to larvae of Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae) as an efficient and effective way of indicating plant defence levels. This generalist herbivore was capable of detecting both inter‐ and intraspecific differences in defence among plant species. The CDD was tested by exploring the effects of various experimental resource conditions (light, nutrients) upon the herbivore preferences and by comparing these preferences with the maximum relative growth rate of plant species. The experimental results provide general support for the CDD hypothesis with respect to nutrient‐level variation but the effects were not related to the origin of the plant species tested. Variation in light conditions did not result in consistent effects upon herbivore preferences. The CDD therefore can be formulated more precisely as: defence levels of plant species vary under different environmental conditions but in a way that is specific for plant species that share evolutionary adaptations to similar nutrient conditions. This more precise CDD hypothesis is a useful addition to existing optimal‐defence theory because of its focus on the possible plastic effects of resource conditions upon plant defence levels. This is relevant when designing experimental plant–herbivore studies.     

Anti-predator defence and the complexity-stability relationship of food webs

The mechanism for maintaining complex food webs has been a central issue in ecology because theory often predicts that complexity (higher the species richness, more the interactions) destabilizes food webs. Although it has been proposed that prey anti-predator defence may affect the stability of prey-predator dynamics, such studies assumed a limited and relatively simpler variation in the food-web structure. Here, using mathematical models, I report that food-web flexibility arising from prey anti-predator defence enhances community-level stability (community persistence and robustness) in more complex systems and even changes the complexity-stability relationship. The model analysis shows that adaptive predator-specific defence enhances community-level stability under a wide range of food-web complexity levels and topologies, while generalized defence does not. Furthermore, while increasing food-web complexity has minor or negative effects on community-level stability in the absence of defence adaptation, or in the presence of generalized defence, in the presence of predator-specific defence, the connectance-stability relationship may become unimodal. Increasing species richness, in contrast, always lowers community-level stability. The emergence of a positive connectance-stability relationship however necessitates food-web compartmentalization, high defence efficiency and low defence cost, suggesting that it only occurs under a restricted condition.     

The evolution of tolerance to deer herbivory: modifications caused by the abundance of insect herbivores

Although recent evidence indicates that coevolutionary interactions between species often vary on a biogeographical scale, little consideration has been given to the processes responsible for producing this pattern. One potential explanation is that changes in the community composition alter the coevolutionary interactions between species, but little evidence exists regarding the occurrence of such changes. Here we present evidence that the pattern of natural selection on plant defence traits, and the probable response to that selection, are critically dependent on the composition of the biotic community. The evolutionary trajectory of defence traits against mammalian herbivory in the Ivyleaf morning glory (Ipomoea hederacea), and which defence traits are likely to respond to selection, are both dependent on the presence or absence of insect herbivores. These results indicate that variation in community composition may be a driving force in generating geographical mosaics.     

运城盐湖群落生物生态学特征研究

运城盐湖植物群落结构简单,种类组成贫乏,总覆盖度20%~80%,变化幅度大,1 m²内仅有优势种1~2个。植物群落类型与土壤含盐量关系密切。同种植物地上部和根部Na⁺含量随土壤盐度的降低而降低,且地上部的降低幅度大于根部。不同种类植物的Na⁺、K⁺、Na/K比含量差异很大。随着土壤盐分的下降,地上部灰分含量也下降。讨论了其可能的变化机制。     

Natural hybridization between Senecio jacobaea and Senecio aquaticus: molecular and chemical evidence

Hybridization is known to be involved in a number of evolutionary processes, including species formation, and the generation of novel defence characteristics in plants. The genus Senecio of the Asteraceae family is highly speciose and has historically demonstrated significant levels of interspecific hybridization. The evolution of novel chemical defence characteristics may have contributed to the success of Senecio hybrids. Chemical defence against pathogens and herbivores has been studied extensively in the model species Senecio jacobaea, which is thought to hybridize in nature with Senecio aquaticus. Here, we use amplified fragment length polymorphisms (AFLPs) and pyrrolizidine alkaloid (PA) composition to confirm that natural hybridization occurs between S. jacobaea and the closely related species S. aquaticus. AFLPs are also used to estimate the ancestry of hybrids. We also demonstrate that even highly back-crossed hybrids can possess a unique mixture of defence chemicals specific to each of the parental species. This hybrid system may therefore prove to be useful in further studies of the role of hybridization in the evolution of plant defence and resistance.     

Adult male emigration and a female-based social organization in swift foxes, Vulpes velox

Members of the family Canidae are distinguished from other carnivore families by pair bonding and male care of the young. Because of the importance of food provisioning and territorial defence by males, social structure among canids is shared or even dominated by males. However, small, insectivorous species of canids show little male parental care, although whether social structure differs from other canids is unknown. We combined data from three independent research projects on a small canid, the swift fox, to help elucidate the social organization of this species. Based on data on movements of 35 adult mated pairs and the fate of litters, we found that adult females maintained territories and family structure, whereas adult males tended to emigrate. This is the first evidence of a female-based social organization among any canid species. This type of social organization probably resulted from the decreased importance of territorial defence and food provisioning by males, as their diet is primarily insectivorous during summer when young are weaned. Our results, along with others, indicate that variations in social structure among canid species are strongly influenced by the importance of food provisioning and territorial defence by males.     

A review of the phytochemical support for the shifting defence hypothesis

Several theories have been developed to explain why invasive species are very successful and develop into pest species in their new area. The shifting defence hypothesis (SDH) argues that invasive plant species quickly evolve towards new defence levels in the invaded area because they lack their specialist herbivores but are still under attack by local (new) generalist herbivores. The SDH predicts that plants should increase their cheap, toxic defence compounds and lower their expensive digestibility reducing compounds. As a net result resources are saved that can be allocated to growth and reproduction giving these plants a competitive edge over the local plant species. We conducted a literature study to test whether toxic defence compounds in general are increased in the invaded area and if digestibility reducing compounds are lowered. We specifically studied the levels of pyrrolizidine alkaloids, a toxin which is known for its beneficial and detrimental impact against specialists and generalists, respectively. Digestibility reducers did not show a clear trend which might be due to the small number of studies and traits measured. The meta analysis showed that toxic compounds in general and pyrrolizidine alkaloid levels specifically, increased significantly in the invaded area, supporting the predictions of the SDH that a fast evolution takes place in the allocation towards defence.     

Host immune defence and migration in birds

Migratory birds are exposed to at least two different parasite faunas during their annual cycle, while resident birds only experience a single parasite fauna. Migratory birds should therefore have evolved mechanisms to control or reduce the negative impact of infections from a more diverse parasite fauna. In a comparison of pairs of closely related species of birds that differ with respect to whether they are migratory or residents, the size of two immune defence organs (the bursa of Fabricius and the spleen) was consistently larger in the migratory species. Since the bursa is only found in juvenile, sexually immature birds, we conclude that immune defence adaptations to the impact of a more diverse parasite fauna in migrants already exist before the start of the first migration. Interspecific differences in investment in immune defence between migratory and resident birds have implications for our understanding of complex host–parasite interactions, the acquisition of new hosts by parasites, and the susceptibility of migratory birds to environmental perturbations.     

One day is enough: rapid and specific host-parasite interactions in a stickleback-trematode system

Red Queen models of host-parasite coevolution are based on genotype by genotype host-parasite interactions. Such interactions require a genotype specific host defence and, simultaneously, a genotype specific parasite infectivity. Specificity is defined here as defence or infection ability successful against only a subset of genotypes of the same species. A specific defence depends on detectable genotypic variation on the parasite side and on a host defence mechanism that differentiates between parasite genotypes. In vertebrates, the MHC-based adaptive immune system can provide such a defence mechanism, but it needs at least several days to get fully mounted. In contrast, the innate immune system is immediately ready. The trematode parasite species used here reaches the immunologically protected eye lens of its three-spined stickleback (Gasterosteus aculeatus) host within 24 h. Thus, it disappears too fast for the fully mounted MHC-based adaptive immune system. In a complete cross-infection experiment using five fish-families and five parasite-clones, we found for the first time fish-family by parasite-clone interactions in vertebrates, although the parasite was only exposed to the immune system for maximally one day. Such interactions require a fast genotype specific defence, suggesting the importance of other defence mechanisms than the too slow, fully mounted adaptive immune system in vertebrates.     

Do Induced Responses Mediate the Ecological Interactions Between the Specialist Herbivores and Phytopathogens of an Alpine Plant?

Plants are not passive victims of the myriad attackers that rely on them for nutrition. They have a suite of physical and chemical defences, and are even able to take advantage of the enemies of their enemies. These strategies are often only deployed upon attack, so may lead to indirect interactions between herbivores and phytopathogens. In this study we test for induced responses in wild populations of an alpine plant (Adenostyles alliariae) that possesses constitutive chemical defence (pyrrolizidine alkaloids) and specialist natural enemies (two species of leaf beetle, Oreina elongata and Oreina cacaliae, and the phytopathogenic rust Uromyces cacaliae). Plants were induced in the field using chemical elicitors of the jasmonic acid (JA) and salicylic acid (SA) pathways and monitored for one month under natural conditions. There was evidence for induced resistance, with lower probability and later incidence of attack by beetles in JA-induced plants and of rust infection in SA-induced plants. We also demonstrate ecological cross-effects, with reduced fungal attack following JA-induction, and a cost of SA-induction arising from increased beetle attack. As a result, there is the potential for negative indirect effects of the beetles on the rust, while in the field the positive indirect effect of the rust on the beetles appears to be over-ridden by direct effects on plant nutritional quality. Such interactions resulting from induced susceptibility and resistance must be considered if we are to exploit plant defences for crop protection using hormone elicitors or constitutive expression. More generally, the fact that induced defences are even found in species that possess constitutively-expressed chemical defence suggests that they may be ubiquitous in higher plants.     

The price of safety: food deprivation in early life influences the efficacy of chemical defence in an aposematic moth

Aposematism is the combination of a primary signal with a secondary defence that predators must learn to associate with one another. However, variation in the level of defence, both within and between species, is very common. As secondary defences influence individual fitness, this variation in quality and quantity requires an evolutionary explanation, particularly as it may or may not correlate with variation in primary signals. The costs of defence production are expected to play a considerable role in generating this variation, yet studies of the cost of chemical defence have focused on species that sequester their defences, while studies in species that produce them de novo are scarce. Here we examine effects of resource availability on the production of chemical defences in female wood tiger moths Arctia plantaginis. This species produces defensive fluids when attacked, and advertises this protection with bright colours on its hindwings. Furthermore, the chemicals in these fluids are produced de novo. In order to establish if the production of this chemical protection is costly, and thus resource‐limited, we manipulated resource availability (i.e. food) during larval development and measured its subsequent effects on adult chemical defence. We presented defensive fluids from female moths to wild blue tits, in the absence of any visual cues, to determine their effectiveness against avian predators. Our results demonstrate that the defensive fluids produced by female moths repel birds, and that these defences require resource investment to produce. We found that moths that were resource‐limited during development had less effective chemical defences, despite producing the same volume of defensive fluids as the control moths. As a reduction in available resources negatively influences the effectiveness of the chemical defence, resource availability may explain the variation seen among individuals.