Phytoplankton defence mechanisms: traits and trade‐offs

In aquatic ecosystems, unicellular algae form the basis of the food webs. Theoretical and experimental studies have demonstrated that one of the mechanisms that maintain high diversity of phytoplankton is through predation and the consequent evolution of defence mechanisms. Proposed defence mechanisms in phytoplankton are diverse and include physiological (e.g. toxicity, bioluminescence), morphological (e.g. silica shell, colony formation), and behavioural (e.g. escape response) traits. However, the function of many of the proposed defence mechanisms remains elusive, and the costs and benefits (trade‐offs) are often unquantified or undocumented. Here, we provide an overview of suggested phytoplankton defensive traits and review their experimental support. Wherever possible we quantify the trade‐offs from experimental evidence and theoretical considerations. In many instances, experimental evidence suggests that defences are costless. However, we argue that (i) some costs materialize only under natural conditions, for example, sinking losses, or dependency on the availability of specific nutrients, and (ii) other costs become evident only under resource‐deficient conditions where a rivalry for limiting resources between growth and defence occurs. Based on these findings, we suggest two strategies for quantifying the costs of defence mechanisms in phytoplankton: (i) for the evaluation of defence costs that are realized under natural conditions, a mechanistic understanding of the hypothesized component processes is required; and (ii) the magnitude of the costs (i.e. growth reduction) must be assessed under conditions of resource limitation.     

Behavioural and toxic effects of termite defensive secretions on ants

ABSTRACT. The toxicity and biological activity of the defensive secretions of ten species of neotropical termites were examined by bioassay on two species of predatory ant. Pseudomyrmex termitarius (F. Smith) (Pseudomyrmecinae) was more susceptible to the effects of the secretions than Ectatomma sp. (Ponerinae). The bioassay results show a progression in the nature of termite chemical weaponry and in the potency of defensive secretions. The tacky secretions used by Coptotermes and Ruptitermes are simply adhesive, entangling agents with no apparent toxic or pheromonal properties. The secretion of Syntermes calvus Emerson serves as a wound-active poison with little topical activity, while those of Armitermes spp. are repellent to ants and show activity as topical poisons. The secretions used by Nasutitermes spp. combine adhesive, entangling properties with the toxicity of a topically-active poison, and are effective also as ant-repellents.     

Optimal investment across different aspects of anti-predator defences

We present a simple model of investment across a suite of different anti-predatory defences. Defences can incur an initial construction cost and and/or may be costly each time they are utilised. Our aim is to use a simple, but general, mathematical model to explore when prey that face a single predatory threat where each attack is of the same nature should invest only in a single defence, and when they should spread their investment across more than one defence. This should help to explain the observed variety of defences that a single prey individual may employ during repeated attacks of a similar nature or even at different stages during one attack. Previous verbal reasoning suggested that prey should specialise in investment in defences that can be utilised early in the predation sequence. Our quantitative model predicts that (depending of the relatively properties of different defences), there may be concentrated investment in early acting, or in late-acting defences, or a spread of investment across both defence types. This variety of predictions is in agreement with the variation in defences shown by natural organisms subjected to repeated predatory attack.     

You get what you pay for: reward-specific trade-offs among direct and ant-mediated defences in plants

Plant defences against herbivores include direct defences such as secondary metabolites or physical structures (e.g. trichomes) as well as indirect defences mediated via mutualistic interactions with other organisms including ants. Production of both direct defences and rewards for mutualistic ants may be costly for a plant, and it has been suggested that trade-offs may exist between direct and ant-mediated defences. We have conducted a meta-analysis of 25 studies testing the above hypothesis and found a significant negative correlation between plant allocation to direct and ant-mediated defences. The strength of correlation was similar for across- and within-species comparisons, and for chemical and physical direct defences. However, trade-offs with direct defences were significant only in plants which offered to ants more costly rewards such as food bodies and/or domatia, but not in plants which attracted ants with relatively cheap extrafloral nectaries. Our results therefore support the hypothesis that plant investment in ant-mediated defences may reduce the requirement for direct chemical and physical defences, but only in plants which offer more costly rewards to their bodyguards.     

Interactions between tomato volatile organic compounds and aphid behaviour

Abstract

In the tritrophic system consisting of tomato, Solanum lycopersicum (L.), the aphid Macrosiphum euphorbiae (Thomas) and its natural enemy, the parasitoid Aphidius ervi (Haliday), it has been shown that the release of volatile organic compounds following aphid attack is responsible for attracting aphid parasitoids in wind tunnel experiments. The main compounds involved in these multitrophic interactions have been characterized and quantified. In this work, the possible activity of such compounds on plant direct defences against the aphid M. euphorbiae was assessed in laboratory tests. The selected compounds were applied to uninfested tomato plants, either by evaporation or contact, and performance of aphids, in terms of plant acceptance, fixing behaviour and aphid development, calculated in standard conditions. The results showed that two compounds, namely methyl salicylate and cis-hex-3-en-1-ol, alter aphid performance. These two compounds have been reported to be those eliciting the best response by A. ervi in terms of flight behavior (wind tunnel bioassay) and antennal stimulation (EAG bioassay).     

Predator-induced changes in morphology of a prey fish: the effects of food level and temporal frequency of predation risk

In a series of experiments, we investigated the effects of food availability and risk frequency on the dynamics of predator-induced changes in growth and morphology of prey fish using goldfish (Carassius auratus) as our test species. In experiment 1, we fed goldfish high or low food rations and exposed them to either alarm cues from conspecifics, cues from swordtails or a water control. After 60 days, goldfish in the alarm cue treatment significantly increased their body depth and body weight but had smaller body length than goldfish exposed to swordtails cues or water, likely reducing their vulnerability to gape-limited predators. Importantly, food level had an impact on the amplitude of the morphological changes. In experiment 2, goldfish were exposed to two different frequencies of predation cues or a water control for 50 days. The cues were either continued or discontinued from day 51 to 100, and all cues were resumed from day 101 to 150. We found that goldfish exposed to predation cues increased their depth and weight at a faster rate than did the goldfish exposed to water, and of particular significance was the fact that frequency of risk had an effect on the amplitude of the change. When the cues were interrupted, the increase in growth rate parameters was reduced to the level of the goldfish exposed to water. However, when the cues were resumed, the rate increased to match the growth rate of the goldfish that were continuously exposed to the cues. Finally, we staged encounters between goldfish of differing morphologies and yellow perch (Perca flavescens) and found that deep-bodied goldfish had better survival than the shallow-bodied ones. These experiments illustrate the dynamic nature of inducible morphological defences.     

An investigation into induced plant defences

This laboratory exercise involves techniques that can be used to investigate induced plant defences. Runner beans are damaged, and the leaves that subsequently grow are tested for the presence of additional defence mechanisms. A control (undamaged) group is kept for comparison. Induced physical defences are indicated by an increase in the density of hairs (trichomes) on the leaves, and induced chemical defences by a decrease in the palatability of the leaves. The latter is tested by a bioassay using garden snails. These basic methods can be used to investigate a variety of defensive responses in plants.     

Silicon-augmented resistance of plants to herbivorous insects: a review

Silicon (Si) is one of the most abundant elements in the earth's crust, although its essentiality in plant growth is not clearly established. However, the importance of Si as an element that is particularly beneficial for plants under a range of abiotic and biotic stresses is now beyond doubt. This paper reviews progress in exploring the benefits at two‐ and three‐trophic levels and the underlying mechanism of Si in enhancing the resistance of host plants to herbivorous insects. Numerous studies have shown an enhanced resistance of plants to insect herbivores including folivores, borers, and phloem and xylem feeders. Silicon may act directly on insect herbivores leading to a reduction in insect performance and plant damage. Various indirect effects may also be caused, for example, by delaying herbivore establishment and thus an increased chance of exposure to natural enemies, adverse weather events or control measures that target exposed insects. A further indirect effect of Si may be to increase tolerance of plants to abiotic stresses, notably water stress, which can in turn lead to a reduction in insect numbers and plant damage. There are two mechanisms by which Si is likely to increase resistance to herbivore feeding. Increased physical resistance (constitutive), based on solid amorphous silica, has long been considered the major mechanism of Si‐mediated defences of plants, although there is recent evidence for induced physical defence. Physical resistance involves reduced digestibility and/or increased hardness and abrasiveness of plant tissues because of silica deposition, mainly as opaline phytoliths, in various tissues, including epidermal silica cells. Further, there is now evidence that soluble Si is involved in induced chemical defences to insect herbivore attack through the enhanced production of defensive enzymes or possibly the enhanced release of plant volatiles. However, only two studies have tested for the effect of Si on an insect herbivore and third trophic level effects on the herbivore's predators and parasitoids. One study showed no effect of Si on natural enemies, but the methods used were not favourable for the detection of semiochemical‐mediated effects. Work recently commenced in Australia is methodologically and conceptually more advanced and an effect of Si on the plants' ability to generate an induced response by acting at the third trophic level was observed. This paper provides the first overview of Si in insect herbivore resistance studies, and highlights novel, recent hypotheses and findings in this area of research. Finally, we make suggestions for future research efforts in the use of Si to enhance plant resistance to insect herbivores.     

Ungulate saliva inhibits a grass–endophyte mutualism

Fungal endophytes modify plant–herbivore interactions by producing toxic alkaloids that deter herbivory. However, studies have neglected the direct effects herbivores may have on endophytes. Antifungal properties and signalling effectors in herbivore saliva suggest that evolutionary pressures may select for animals that mitigate the effects of endophyte-produced alkaloids. Here, we tested whether saliva of moose (Alces alces) and European reindeer (Rangifer tarandus) reduced hyphal elongation and production of ergot alkaloids by the foliar endophyte Epichloë festucae associated with the globally distributed red fescue Festuca rubra. Both moose and reindeer saliva reduced the growth of isolated endophyte hyphae when compared with a treatment of distilled water. Induction of the highly toxic alkaloid ergovaline was also inhibited in plants from the core of F. rubra''s distribution when treated with moose saliva following simulated grazing. In genotypes from the southern limit of the species'' distribution, ergovaline was constitutively expressed, as predicted where growth is environmentally limited. Our results now present the first evidence, to our knowledge, that ungulate saliva can combat plant defences produced by a grass–endophyte mutualism.     

The interaction between maternal stress and the ontogeny of the innate immune system during teleost embryogenesis: implications for aquaculture practice

The barrier defences and acellular innate immune proteins play critical roles during the early‐stage fish embryos prior to the development of functional organ systems. The innate immune proteins in the yolk of embryos are of maternal origin. Maternal stress affects the maternal‐to‐embryo transfer of these proteins and, therefore, environmental stressors may change the course of embryo development, including embryonic immunocompetency, via their deleterious effect on maternal physiology. This review focuses on the associations that exist between maternal stress, maternal endocrine disturbance and the responses of the acellular innate immune proteins of early‐stage fish embryos. Early‐stage teleostean embryos are dependent upon the adult female for the formation of the zona pellucida as an essential barrier defence, for their supply of nutrients, and for the innate immunity proteins and antibodies that are transferred from the maternal circulation to the oocytes; maternally derived hormones are also transferred, some of which (such as cortisol) are known to exert a suppressive action on some aspects of the immune defences. This review summarizes what is known about the effects of oocyte cortisol content on the immune system components in early embryos. The review also examines recent evidence that embryonic cells during early cleavage have the capacity to respond to increased maternal cortisol transfer; this emphasizes the importance of maternal and early immune competence on the later life of fishes, both in the wild and in intensive culture.     

Below‐ground nematode herbivory of resistant soybean cultivars impairs the performances of an above‐ground caterpillar and its parasitoid

1. Interactions between below‐ and above‐ground organisms have attracted interest in recent years, but less is known about the effect of root‐feeding nematodes on above‐ground trophic interactions between herbivores and their natural enemies. 2. This study examined whether the presence of the soybean cyst root nematode Heterodera glycines influences the performance of the above‐ground leaf‐chewing tobacco cutworm Spodoptera litura on soybeans, Glycine max, and whether this in turn affects the success of its parasitoid, Meteorus pulchricornis. Using three soybean cultivars that varied in the level of constitutive resistance to the tobacco cutworm, the study determined whether feeding by the nematode altered the developmental and reproductive performances of the caterpillar and its parasitoid. 3. Root feeding by the nematode slowed tobacco cutworm larval development time and reduced adult body weight. Root feeding by the nematode also had a negative effect on the caterpillar's parasitoid, by prolonging development time, decreasing adult body size and reducing fecundity. These effects increased in a linear trend and varied in magnitude depending on levels of soybean constitutive resistance. 4. These findings demonstrate that root feeding by the nematode can prime soybean plants with negative impacts on their herbivore and its parasitoid, and that the impact may vary in magnitude depending on levels of soybean constitutive defence. The results emphasise the need to integrate soybean constitutive and root nematode‐induced defences for a better understanding of below‐ and above‐ground organism interactions, and to allow insights to be gained into the improvement of soybean integrated pest management programmes.     

Scraping a living: a review of littorinid grazing

Littorinid snails are predominantly herbivorous and the versatility of their radulae enables them to feed on a variety of macroscopic and microscopic plants in a diversity of habitats. Some are selective feeders preferring some species of algae to others, and rejecting some even after a prolonged period of starvation. Different species of snail exhibit different preferences. The factors affecting the attractiveness and edibility of food plants are discussed and food value considered.Foraging behaviour of littorinids is briefly reviewed in relation to the influence of chemical cues from the algae. Littorinids appear to be able to select or reject algae without having ingested them, having perceived the plants from a distance, moving towards favoured foods (or habitat-providing plants) and away from those that it rejects. The nature of the chemical cues emitted by the algae is discussed. Temporal patterns of foraging activity show some evidence of an endogenous component which can be overridden by responses to environmental conditions. These patterns place restraints on energy intake.The structural and chemical defences used by algae against littorinid grazing are considered. The importance of polyphenolic compounds is evaluated. The effects of grazing as a selective agency and a factor influencing algal populations are discussed. There is some evidence that life history patterns are a response to grazing. The influence of external physical factors, such as salinity on grazing pressure is demonstrated.Finally, the impact of littorinid snails on intertidal communities is assessed in relation to their abundance and biogeographical distribution. The relative importance of littorinids is contrasted on shores possessing or lacking limpets.     

Why are so many trees hollow?

In many living trees, much of the interior of the trunk can be rotten or even hollowed out. Previously, this has been suggested to be adaptive, with microbial or animal consumption of interior wood producing a rain of nutrients to the soil beneath the tree that allows recycling of those nutrients into new growth via the trees roots. Here I propose an alternative (non-exclusive) explanation: such loss of wood comes at very little cost to the tree and so investment in costly chemical defence of this wood is not economic. I discuss how this theory can be tested empirically.     

Physical and chemical response of juvenile Acacia tortilis trees to browsing. Experimental evidence

1. Changes in nutritional value and accessibility of leaves following browsing are important in the dynamics of plant–herbivore interactions because they influence the fitness of the plant attacked and the future utilization of it by the herbivore.
2. Hand pruning of Acacia tortilis , a spinescent tree common in savanna ecosystems of eastern Africa, resulted in higher biomass of spines and new shoots in pruned trees than in unpruned controls.
3. Pruned trees allocated a higher proportion of shoot biomass to spines than unpruned ones, whereas the proportion of leaf biomass in new shoots was slightly reduced. Because increases in spine biomass and density following pruning are coupled with an increase in shoot production, it is concluded that higher production of spines is an inducible response of Acacia tortilis to pruning.
4. No significant changes in the concentration of total phenolics, condensed tannins or leaf nitrogen were induced by pruning.
5. Irrespective of treatment, high foliar concentrations of nitrogen were correlated with an increase in twig production for a given leaf biomass and a reduction in the concentration of secondary substances in leaves. This relation may lead to a conflict between foraging efficiency and nutrition for browsers of A. tortilis.     

Impacts of silica-based defences in grasses on the feeding preferences of sheep

Grasses, which dominate many terrestrial ecosystems, sustain high densities of grazing mammals, so are of great economic and ecological importance. Traditionally, grasses are thought to be adapted to tolerate grazing rather than defend against it; however, silica deposited in the leaves of grasses has recently been shown to act as a feeding deterrent to invertebrate herbivores and small mammals. This study assesses whether silica is effective as a feeding deterrent to larger mammalian herbivores. We assess the impact of manipulated silica levels in five grass species on the feeding preferences of sheep both within and between grass species.Sheep feeding behaviour was driven by between-species differences in palatability. Hence, within a single species silica addition did not cause significant changes in feeding preference. However, there were significant differences in both the feeding preferences and bite rates between grass species, and these differences were much more marked when the grasses had been exposed to high levels of silica. The impacts that silica had on preference were least pronounced in palatable species (e.g. Poa annua) compared with less-palatable species (e.g. Brachypodium pinnatum and Festuca ovina). Sheep fed for longer, took more bites and had a higher bite rate on the grass species with the lowest leaf silica concentrations, namely P. annua.Sheep were less affected by silica defences than smaller, non-ruminant herbivores, but the changes in species preference rankings caused by silica suggest it may lead to changes in sward composition. Further, in species that are already relatively low in palatability, silica-induced reductions in bite rate could potentially reduce forage intake rates, with consequences for sheep performance.     

Diverse strategies that animals use to deter intraspecific predation

Intraspecific predation is a special case of prey–predator system that is taxonomically widespread. While a heterospecific predator's main goal is to achieve nutrition, intraspecific predation provides conspecifics with other benefits including elimination of competitors for resources and mates. Traditionally intraspecific predation is termed based on the context they occur within, for example egg cannibalism, infanticide and sexual cannibalism. These diverse forms of intraspecific predation and the strategies by which animals are known to deter them are summarized categorically in this review. The diversity of defence strategies animals deploy against conspecific predators is appreciable and raises interesting questions on their evolution for future research.     

Induction of different defences by two enemies in the rotifer Keratella tropica: response priority and sensitivity to enemy density

1. Keratella tropica has qualitatively distinct spine‐development responses to kairomones released by the predatory rotifer Asplanchna and the cladoceran interference competitor Daphnia. Asplanchna induces a fourfold lengthening of the right posterior spine (to c.100 μm), a shortening or loss of the left posterior spine and a lengthening of two pairs of anterior spines. Daphnia induces a moderate elongation of both right and left posterior spines. This study tests three hypotheses regarding the sensitivity of these responses to enemy density, and the response priority when both enemies are present. 2. First, since K. tropica and Brachionus calyciflorus have similarly pronounced and effective spine‐development responses to Asplanchna, with no appreciable demographic cost, they should be similarly sensitive to Asplanchna density. This was the case. Both showed an exponential response to increasing Asplanchna density, well described by an asymptotic exponential regression model, and exhibited 50% maximal spine development at statistically similar Asplanchna densities–2.5 and 1.7 μg dry weight L^?1 (1.8 and 1.2 individuals L^?1), respectively. Strong selection for these Asplanchna‐induced responses clearly has led to a coupling of exuberant and effective morphological defence with an unrivalled sensitivity to predator density. 3. Second, since K. tropica’s response to Daphnia is much less pronounced and effective than its response to Asplanchna, it should be less sensitive to Daphnia density. This hypothesis was supported. Spine development increased linearly with increasing Daphnia density and was 50% maximal at 454 μg dry weight Daphnia L^?1, a biomass density 180 times greater than that inducing a comparable response to Asplanchna. 4. Third, since K. tropica’s response to Daphnia does not reduce Asplanchna predation, K. tropica should respond to Asplanchna when both enemies are present at densities sufficient to induce spine development. This was the case. The presence of Daphnia neither reduced nor increased the length of the right posterior spine; it only limited the extent to which the left spine was reduced or lost.     

The sight of an adult brood parasite near the nest is an insufficient cue for a honeyguide host to reject foreign eggs

Hosts of brood‐parasitic birds typically evolve anti‐parasitism defences, including mobbing of parasitic intruders at the nest and the ability to recognize and reject foreign eggs from their clutches. The Greater Honeyguide Indicator indicator is a virulent brood parasite that punctures host eggs and kills host young, and accordingly, a common host, the Little Bee‐eater Merops pusillus frequently rejects entire clutches that have been parasitized. We predicted that given the high costs of accidentally rejecting an entire clutch, and that the experimental addition of a foreign egg is insufficient to induce this defence, Bee‐eaters require the sight of an adult parasite near the nest as an additional cue for parasitism before they reject a clutch. We found that many Little Bee‐eater parents mobbed Greater Honeyguide dummies while ignoring barbet control dummies, showing that they recognized them as a threat. Surprisingly, however, neither a dummy Honeyguide nor the presence of a foreign egg, either separately or in combination, was sufficient to stimulate egg rejection.