Induced defences in marine and freshwater phytoplankton: a review

Many organisms have developed defences to avoid predation by species at higher trophic levels. The capability of primary producers to defend themselves against herbivores affects their own survival, can modulate the strength of trophic cascades and changes rates of competitive exclusion in aquatic communities. Algal species are highly flexible in their morphology, growth form, biochemical composition and production of toxic and deterrent compounds. Several of these variable traits in phytoplankton have been interpreted as defence mechanisms against grazing. Zooplankton feed with differing success on various phytoplankton species, depending primarily on size, shape, cell wall structure and the production of toxins and deterrents. Chemical cues associated with (i) mechanical damage, (ii) herbivore presence and (iii) grazing are the main factors triggering induced defences in both marine and freshwater phytoplankton, but most studies have failed to disentangle the exact mechanism(s) governing defence induction in any particular species. Induced defences in phytoplankton include changes in morphology (e.g. the formation of spines, colonies and thicker cell walls), biochemistry (such as production of toxins, repellents) and in life history characteristics (formation of cysts, reduced recruitment rate). Our categorization of inducible defences in terms of the responsible induction mechanism provides guidance for future work, as hardly any of the available studies on marine or freshwater plankton have performed all the treatments that are required to pinpoint the actual cue(s) for induction. We discuss the ecology of inducible defences in marine and freshwater phytoplankton with a special focus on the mechanisms of induction, the types of defences, their costs and benefits, and their consequences at the community level.     

Induced systemic resistance (ISR) against pathogens in the context of induced plant defences

Induced systemic resistance (ISR) of plants against pathogens is a widespread phenomenon that has been intensively investigated with respect to the underlying signalling pathways as well as to its potential use in plant protection. Elicited by a local infection, plants respond with a salicylic-dependent signalling cascade that leads to the systemic expression of a broad spectrum and long-lasting disease resistance that is efficient against fungi, bacteria and viruses. Changes in cell wall composition, de novo production of pathogenesis-related-proteins such as chitinases and glucanases, and synthesis of phytoalexins are associated with resistance, although further defensive compounds are likely to exist but remain to be identified. In this Botanical Briefing we focus on interactions between ISR and induced resistance against herbivores that is mediated by jasmonic acid as a central signalling molecule. While many studies report cross-resistance, others have found trade-offs, i.e. inhibition of one resistance pathway by the other. Here we propose a framework that explains many of the thus far contradictory results. We regard elicitation separately from signalling and from production, i.e. the synthesis of defensive compounds. Interactions on all three levels can act independently from each other.     

Induced defences in an endangered amphibian in response to an introduced snake predator

Introduced species have contributed significantly to the extinction of endemic species on islands. They also create new selection pressures on their prey that may result in modified life history strategies. Introduced viperine snakes (Natrix maura) have been implicated in the decline of the endemic midwife toad of Mallorca (Alytes muletensis). A comparison of A. muletensis tadpoles in natural pools with and without snakes showed that those populations subject to snake predation possessed longer tails with narrower tail fins but deeper tail muscles. Field and laboratory experiments showed that these changes in tail morphology could be induced by chemical and tactile cues from snakes. Populations of tadpoles that were subject to snake predation also displayed clear bimodal size-frequency distributions, with intermediate-sized tadpoles missing from the pools completely. Tadpoles in pools frequented by snakes developed faster in relation to their body size than those in pools without snakes. Variation in morphology between toad populations may therefore be caused by a combination of size-selective predation and tadpole plasticity. The results of this study indicate that the introduction of alien species can result in selection for induced defences, which may facilitate coexistence between predator and prey under certain conditions.     

Induced defences alter the strength and direction of natural selection on reproductive traits in common milkweed

Evolutionary biologists have long sought to understand the ecological processes that generate plant reproductive diversity. Recent evidence indicates that constitutive antiherbivore defences can alter natural selection on reproductive traits, but it is unclear whether induced defences will have the same effect and whether reduced foliar damage in defended plants is the cause of this pattern. In a factorial field experiment using common milkweed, Asclepias syriaca L., we induced plant defences using jasmonic acid (JA) and imposed foliar damage using scissors. We found that JA‐induced plants experienced selection for more inflorescences that were smaller in size (fewer flowers), whereas control plants only experienced a trend towards selection for larger inflorescences (more flowers); all effects were independent of foliar damage. Our results demonstrate that induced defences can alter both the strength and direction of selection on reproductive traits, and suggest that antiherbivore defences may promote the evolution of plant reproductive diversity.     

Inducible chemical defences in animals

Phenotypic plasticity is extremely widespread in the behaviour, morphology and life‐history of animals. However, inducible changes in the production of defensive chemicals are described mostly in plants and surprisingly little is known about similar plasticity in chemical defences of animals. Inducible chemical defences may be common in animals because many are known to produce toxins, the synthesis of toxins is likely to be costly, and there are a few known cases of animals adjusting their toxin production to changes in environmental conditions. We outline what is known about the occurrence of inducible chemical defences in animals and argue that there is immense potential for progress in this field. Possible directions include surveying diverse taxa to explore how general its occurrence may be and testing for selection acting on inducible chemical defences. Data on inducible chemical defences would provide insight into life‐history tradeoffs by enabling novel tests of how time‐costs and resource‐costs affect life‐history. If the synthesis of toxic compounds by animals proves accessible to manipulation, as it is in plants and fungi, this will open the way to refined estimates of the fitness costs of defence, ultimately providing a clearer picture of how plasticity evolves and is maintained in nature. Synthesis Inducible changes in the behaviour, morphology, and life‐history of animals are extremely widespread, but surprisingly little is known about similar changes in the production of defensive chemicals. We outline what is known about the occurrence of inducible chemical defences in animals and argue that there is immense potential for progress in this field. Possible directions include surveying diverse taxa to explore how general its occurrence may be and testing for selection acting on inducible chemical defences. Data on inducible chemical defences would provide insight into life‐history tradeoffs by enabling novel tests of how time‐costs and resource‐costs affect life‐history. If the synthesis of toxic compounds by animals proves accessible to manipulation, we will be able to estimate the fitness costs of defence more precisely, and ultimately provide a clearer picture of how plasticity evolves and is maintained in nature.     

Induced defences in the neotropical tree Bauhinia brevipes (Vog.) to herbivory: effects of damage-induced changes on leaf quality and insect attack

Induced defences to herbivory are physical, nutritional, and allelochemical traits that change in plants following damage or stress, and that reduce the performance and/or preference of herbivores. The aim of this study was to verify the occurrence and effect of induced responses in Bauhinia brevipes (Vog.) (Leguminosae) which defend it against herbivores, through the manipulation of its leaves, and their effects on herbivore foraging behaviour. We selected 15 plants in the field, and three shoots per plant were subjected to one of three treatments: (1) damaged shoots (simulation of the main types of foliar herbivory and insect exclusion); (2) damaged control shoots (insect exclusion); and (3) control shoots (not manipulated). Water and nitrogen content, tannin concentration, levels of herbivory, and shoot growth rates were compared among treatments. Leaf quality varied among treatments. Damaged leaves showed higher tannin concentration, and lower water and nitrogen content compared to undamaged leaves. On the other hand, they experienced higher rates of herbivory than leaves on control shoots. Moreover, shoots that were experimentally induced showed a higher increase in final shoot length. These results suggest that simulated herbivory on B. brevipes reduced the nutritional quality of its leaves and increased the amount of secondary compounds, therefore altering insect herbivore attack and increasing shoot performance.     

Development of predator defences in fishes

Summary A variety of development characteristics, morphological, behavioural, and experiential, contribute to the extreme vulnerability of young fishes to predation. The influence of these characteristics is complicated by the fact that the larval period is one of substantial and rapid change. Yet survival is the ultimate goal;-it is only by reaching maturity that individual fish have the opportunity to reproduce. With such high stakes it is not surprising that predator defences are of major importance during all phases of life. Developmental constraints may limit the defensive options for young fishes. Avoidance behaviours, which reduce the likelihood of encountering a predator or of being attacked by it, are particulaly evident in the youngest stages. Here size, coloration and dispersal are used to help elude the predator's attention. As fishes grow and acquire greater morphological and behavioural sophistication, there is more scope for predator evasion when avoidance fails. Older fishes are increasingly able to respond to external stimuli and can detect and react to predators or join conspecifics in common defence (schooling). Behavioural development is not simply a consequence of growth and the concomitant physical alterations of the body; it is also mediated by experience that comes through interaction with the physical and biotic environment. Predispositions to respond to experience may be a product of evolutionary history. Although mortality rates decline markedly with development and maturity, changes in size or behaviour can render fishes vulnerable to new suites of predators. Effective predator avoidance can compromise other activities, such as foraging, and individuals may be forced to reconcile conflicting demands. Developmental niche shifts that occur, for example, when certain size classes take refuge in less profitable feeding habitats, represent one such trade-off. Niche shifts may also be mediated by the influence of the programme for morphological development on sensory or behavioural capabilities. In addition to all of these developmental consderations, natural variations in environmental conditions — such as temperature, photoperiod, predator density and variety, and presence of alternative prey — represent additional challenges to predator defences during the rite of passage from birth to reproduction.     

Trade-off among antiherbivore defences in a south american blackberry (Rubus bogotensis)

Summary The idea of trade-offs among antiherbivore defences in plants is examined using data from a South American blackberry (Rubus bogotensis). Two distinct morphs of R. bogotensis, one with glandular trichomes and one without, were compared with respect to leaf toughness, number of prickles and prickle length. The two morphs were sympatric and grew under similar environmental conditions. The morph lacking trichomes had significantly tougher leaves and also tended to have more and longer prickles. Bioassay showed that Ithomiid larvae fed to a lesser extent on tough leaves than on more tender ones. Correlations between antiherbivore defences within each phenotype revealed three significant or almost significant negative relationships. The comparisons support the hypothesis that trade-offs exist among antiherbivore defences.     

Innate immune defences in the human endometrium

The human endometrium is an important site of innate immune defence, giving protection against uterine infection. Such protection is critical to successful implantation and pregnancy. Infection is a major cause of preterm birth and can also cause infertility and ectopic pregnancy. Natural anti-microbial peptides are key mediators of the innate immune system. These peptides, between them, have anti-bacterial, anti-fungal and anti-viral activity and are expressed at epithelial surfaces throughout the female genital tract. Two families of natural anti-microbials, the defensins and the whey acidic protein (WAP) motif proteins, appear to be prominent in endometrium. The human endometrial epithelium expresses beta-defensins 1–4 and the WAP motif protein, secretory leukocyte protease inhibitor. Each beta-defensin has a different expression profile in relation to the stage of the menstrual cycle, providing potential protection throughout the cycle. Secretory leukocyte protease inhibitor is expressed during the secretory phase of the cycle and has a range of possible roles including anti-protease and anti-microbial activity as well as having effects on epithelial cell growth. The leukocyte populations in the endometrium are also a source of anti-microbial production. Neutrophils are a particularly rich source of alpha-defensins, lactoferrin, lysozyme and the WAP motif protein, elafin. The presence of neutrophils during menstruation will enhance anti-microbial protection at a time when the epithelial barrier is disrupted. Several other anti-microbials including the natural killer cell product, granulysin, are likely to have a role in endometrium. The sequential production of natural anti-microbial peptides by the endometrium throughout the menstrual cycle and at other sites in the female genital tract will offer protection from many pathogens, including those that are sexually transmitted.     

Herbivore-induced, indirect plant defences

Indirect responses are defensive strategies by which plants attract natural enemies of their herbivores that act as plant defending agents. Such defences can be either constitutively expressed or induced by the combined action of mechanical damage and low- or high-molecular-weight elicitors from the attacking herbivore. Here, we focus on two induced indirect defences, namely the de novo production of volatiles and the secretion of extrafloral nectar, which both mediate interactions with organisms from higher trophic levels (i.e., parasitoids or carnivores). We give an overview on elicitors, early signals, and signal transduction resulting in a complex regulation of indirect defences and discuss effects of cross-talks between the signalling pathways (synergistic and antagonistic effects). In the light of recent findings, we review molecular and genetic aspects of the biosynthesis of herbivore-induced plant volatiles comprising terpenoids, aromatic compounds, and metabolites of fatty acids which act as infochemicals for animals and some of which even induce defence genes in neighbouring plants. Finally, ecological aspects of these two indirect defences such as their variability, specificity, evolution as well as their ecological relevance in nature are discussed.     

Environmental calcium modifies induced defences in snails

Inducible defences are adaptive phenotypes that arise in response to predation threats. Such plasticity incurs costs to individuals, but there has been little interest in how such induced traits in animals may be constrained by environmental factors. Here, we demonstrate that calcium availability interacts with predation cues to modify snail shell growth and form. Small snails increased their growth and were heavier when exposed to fish chemical cues, but this response was calcium limited. There was also an interactive effect of fish cues and calcium on the shell growth of larger snails, but shell strength and aperture narrowness were affected by calcium alone. For small snails, behavioural avoidance was greatest for snails exhibiting least morphological plasticity, suggesting a trade-off. There was no trade-off of somatic growth with plasticity. We suggest that the expression of defensive traits in molluscs can be constrained by calcium availability, which has implications for molluscan ecology and evolution.     

Antimicrobial defences increase with sociality in bees

Evidence for the antiquity and importance of microbial pathogens as selective agents is found in the proliferation of antimicrobial defences throughout the animal kingdom. Social insects, typified by crowding and often by low genetic variation, have high probabilities of disease transmission and eusocial Hymenoptera may be particularly vulnerable because of haplodiploidy. Mechanisms they employ to reduce the risk of disease include antimicrobial secretions which are particularly important primary barriers to infection. However, until now, whether or not there is selection for stronger antimicrobial secretions when the risk of disease increases because of sociality has not been tested. Here, we present evidence that the production of progressively stronger antimicrobial compounds was critical to the evolution of sociality in bees. We found that increases in group size and genetic relatedness were strongly correlated with increasing antimicrobial strength. The antimicrobials of even the most primitive semi-social species were an order of magnitude stronger that those of solitary species, suggesting a point of no return, beyond which disease control was essential. Our results suggest that selection by microbial pathogens was critical to the evolution of sociality and required the production of strong, front-line antimicrobial defences.     

Antioxidant defences of the apoplast

Summary The apoplast of barley and oat leaves contained superoxide dismutase (SOD), catalase, ascorbate peroxidase, dehydroascorbate reductase, monodehydroascorbate reductase, and glutathione reductase activities. The activities of these enzymes in the apoplastic extracts were greatly modified 24 h after inoculation with the biotrophic fungal pathogenBlumeria graminis. The quantum efficiency of photosystem II, which is related to photosynthetic electron transport flux, was comparable in inoculated and healthy leaves during this period. Apoplastic soluble acid invertase activity was also modified in inoculated leaves. Inoculation-dependent increases in apoplastic SOD activity were observed in all lines. Major bands of SOD activity, observed in apoplastic protein extracts by activity staining of gels following isoelectric focusing, were similar to those observed in whole leaves but two additional minor bands were found in the apoplastic fraction. The apoplastic extracts contained substantial amounts of dehydroascorbate (DHA) but little or no glutathione (GSH). Biotic stress decreased apoplastic ascorbate and DHA but increased apoplastic GSH in resistant lines. The antioxidant cycle enzymes may function to remove apoplastic H₂O₂ with ascorbate and GSH derived from the cytoplasm. DHA and oxidized glutathione may be reduced in the apoplast or returned to the cytosol for rereduction.Abbreviations AA reduced ascorbate - APX ascorbate peroxidase - DHA dehydroascorbate (oxidised ascorbate) - DHAR dehydroascorbate reductase - G6PDH glucose-6-phosphate dehydrogenase - GSH reduced glutathione - GSSG glutathione disulphide - GR glutathione reductase - MDHA monodehydroascorbate - MDHAR monodehydroascorbate reductase - SOD superoxide dismutase