Low nutritive quality as a plant defence: Effects of herbivore-mediated interactions

Summary A plant may lower its nutritive quality, for herbivores, by using secondary compounds, morphological characters and/or having a lowered nutrient content. If such traits decrease the amount of resources lost through herbivory, then they act as antiherbivore defences. However, if herbivores compensate for the lowered nutrient availability, by increasing their intake rates or by prolonging their feeding periods, then this may render the defence useless. I analyse the conditions for evolution of this type of plant defences in a game theoretical model. The predictions of the model depend on the amount of compensatory feeding performed by the herbivores and on the herbivores' mobility in relation to the spatial structure of the plant population. When herbivores cannot compensate for a lowered nutritive quality, the defence can evolve irrespective of the type of herbivore. When herbivores can compensate for such defences, the outcome depends on how the herbivores compensate. In situations where herbivores compensate only on defended plants, which could correspond to immobile herbivores, this type of defence can evolve only if the level of compensation is lower than a certain critical value. When herbivores compensate more on defended than on undefended plants, e.g. because of low mobility, the outcome depends on the level of compensation performed on defended plants. If this level of compensation is high, then the model predicts a stable coexistence of defended and undefended plants and, if it is low, then the populations can consist of only defended plants. When herbivores compensate more on undefended plants than on defended ones, e.g. highly mobile herbivores, the result is populations consisting of either only defended plants, or only undefended plants. Consequently, the fact that herbivores may compensate for lowered nutrient quality does not, as such, nullify the notion of low nutrient quality as a plant defence. However, compensatory feeding may restrict the conditions for the evolution of such defences.     

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.     

Remobilised nitrogen and root uptake of nitrate for spring leaf growth,flowers and developing fruits of pear (Pyrus communis L.) trees

Both uptake of fertiliser N and remobilisation of stored N were quantified for the early growth of spur and shoot leaves, flowers and fruit development of pear trees. One-year old Abbé F. trees grafted on quince C rootstocks were fertilised with a generous N supply for one year and while dormant during the winter, transferred to sand cultures. Each tree received 3 g of labelled nitrate-N at the end of winter and in early spring. Leaves, flowers and fruit were sampled on 5 separate occasions and the recovery of labelled N used to distinguish the remobilisation of N and the root uptake of nitrate. Remobilisation of stored N accounted for most of the N present in leaves and flowers during blossoming. Remobilisation of nitrogen stopped between petal fall and the beginning of fruit development. Root uptake of nitrate linearly increased over time and at the last sampling, 55 days after bud burst, fertiliser N contributed approximately half of the total N recovered in both spur and shoot leaves, the remainder coming from remobilisation. Flowers and fruits based their N metabolism more on remobilisation as compared to the leaves. This pattern of internal cycling of N is discussed in relation to fertilisation strategies for pear trees.     

The evolution of warning signals as reliable indicators of prey defense

It is widely argued that defended prey have tended to evolve conspicuous traits because predators more readily learn to avoid defended prey when they are conspicuous. However, a rival theory proposes that defended prey have evolved such characters because it allows them to be distinguished from undefended prey. Here we investigated how the attributes of defended (unprofitable) and undefended (profitable) computer-generated prey species tended to evolve when they were subject to selection by foraging humans. When cryptic forms of defended and undefended species were similar in appearance but their conspicuous forms were not, defended prey became conspicuous while undefended prey remained cryptic. Indeed, in all of our experiments, defended prey invariably evolved any trait that enabled them to be distinguished from undefended prey, even if such traits were cryptic. When conspicuous mutants of defended prey were extremely rare, they frequently overcame their initial disadvantage by chance. When Batesian mimicry of defended species was possible, defended prey evolved unique traits or characteristics that would make undefended prey vulnerable. Overall, our work supports the contention that warning signals are selected for their reliability as indicators of defense rather than to capitalize on any inherent educational biases of predators.     

Defensive traits of savanna trees – the role of shoot exposure to browsers

To investigate patterns of plant defence, a study was conducted on 13 tree species in Botswana. We tested the hypotheses that (1) shoots on small, young trees are more defended than shoots at the same height on tall, mature individuals and (2) shoots within browsing height are more defended than shoots above the reach of browsers, on mature trees. Plant traits studied were total phenolics, tannin activity, nitrogen (N), acid-detergent fibre (ADF), and degree of spinescence (in three species). We found some support for the first hypothesis. Overall young trees had a significantly higher concentration of total phenolics than mature trees and on species level these differences were significant for three of the 13 species. However, we found no differences in tannin activity, spinescence or ADF concentration between young and mature trees, and four species had higher levels of N in young trees, suggesting higher overall palatability. Contrary to our second hypothesis, shoots within browsing height were less chemically defended (total phenolics and tannin activity) than shoots above browsing height in six of 13 species. Two species had less ADF in lower shoots, and no significant differences were found in N or spinescence for any species. This study included a broad range of tree species at two sites and the results indicate that general theories of plant defence, originating from boreal and northern temperate forests, cannot be simply applied to savanna ecosystems.     

Costs and limits of dosage response to predation risk: to what extent can tadpoles invest in anti-predator morphology?

Inducible defences have long been considered as a polyphenism opposing defended and undefended morphs. However, in nature, preys are exposed to various levels of predation risk and scale their investment in defence to actual predation risk. Still, among the traits that are involved in the defence, some are specific to one predator type while others act as a more generalised defence. The existence of defence costs could prevent an individual investing in all these traits simultaneously. In this study, we investigate the impact of an increasing level of predator density (stickleback, Gasterosteus aculeatus) on the expression of morphological inducible defences in tadpoles of Rana dalmatina. In this species, investment in tail length and tail muscle is a stickleback-specific response while increased tail fin depth is a more general defence. As expected, we found a relationship between investment in defence and level of risk through the responses of tail fin depth and tail length. We also found an exponential increase of defence cost, notably expressed by convex decrease of growth and developmental rates. We found a relative independence of investment in the different traits that compose the defence, revealing a high potential for fine tuning the expression of defended phenotypes with respect to local ecological conditions.     

Facilitation by herbivore-mediated nurse plants in a threatened tree, Taxus baccata: local effects and landscape level consistency

We investigated the regeneration of a threatened tree, the yew Taxus baccata, in relation to the presence of fleshy‐fruited woody plants acting as seed dispersal foci as well as protecting yew recruits against ungulate herbivores. We seek to determine if local facilitative effects are consistent across landscape in the Cantabrian range (NW Spain). Yew seed rain by birds mostly concentrated under yew trees and beneath hollies Ilex aquifolium. Seedling emergence distributed similarly to seed rain, but first‐year seedling survival was higher beneath hollies. In one site where woody vegetation was structured as nucleation centres (multispecific patches of fleshy‐fruited plants acting as foci for seed rain) yew recruits mostly occurred in yew‐dominated centres, suggesting dispersers‐mediated facilitation. However, holly was the main nurse plant for most of these recruits, considering the nurse as the species whose canopy covered directly the yew recruit. Living beneath nurse plants reduced herbivore damage on saplings and enhanced seedling survival. A planting experiment with yew rooted‐cuttings beneath different spiny shrubs corroborated this effect. Additional evidence on yew recruitment limitation by herbivory emerged from one population where ungulates were fence‐excluded. Our results suggest that nurse plants mitigate the negative effect of herbivores on yew regeneration, by providing defence against browsing and trampling. Shelter ability related to nurse structure, cone‐shaped shrubs with branches at their bases acting better as a barrier. Paradoxically, this structure resulted from heavy browsing on nurse plants. The study of yew regeneration and habitat structure in seven sites provided evidence for the consistency of facilitation by holly at the landscape level, since local values of yew recruitment positively related to nurse ground cover. Range‐scale yew management must consider the local functioning of the interaction among avian seed‐dispersers, nurse fleshy‐fruited plants and ungulate herbivores, in combination with regional measures, targeting the habitats where facilitation emerges.     

Plant defence signals and Batesian mimicry

In a game theory context, we investigated conditions for an evolutionarily stable equilibrium of defended, signalling plants, and plants mimicking these signals – that is, conditions for a stable mimicry complex. We modelled this in three steps. First, we analysed conditions for selection for defended, signalling plants, in a population of undefended plants. Second, we analysed conditions for when mimicking plants can invade a population of defended, signalling plants, leading to a stable equilibrium between the two strategies. Third, we analysed how sampling of signalling plants by herbivores affects the equilibrium between the strategies. The predictions show that mimicry of plant defence signals may be common, and even imperfect mimics could invade a population of defended, signalling plants. Whether the latter prediction holds or not depends on how herbivores generalize over signals, and on the length of their avoidance sequence'. The length of the avoidance sequence is the number of signalling plants that a herbivore avoids to attack, after attacking a defended plant. If herbivores always sample signalling plants, then mimicry cannot evolve, whereas if herbivores have a long avoidance sequence, this may allow selection even for imperfect mimics.     

Experimental fruit removal does not affect territory structure of wintering Hermit Thrushes

ABSTRACT.   Food is generally considered to be the primary resource structuring winter territories in migrant songbirds, but there is little experimental evidence to support this. In southeastern Louisiana, ripe fruits, consumed opportunistically in the absence of preferred arthropod resources, are a primary food resource for wintering Hermit Thrushes ( Catharus guttatus ). To test the possible role of food in controlling space use during the winter, we reduced fruit availability in the territories of wintering Hermit Thrushes and compared responses of these thrushes to those in control territories where fruit availability was not altered. We found that thrushes did not adjust either territory size or location in response to midwinter reduction of fruit availability. One possible explanation for this lack of response is that sufficient food, including arthropods, was available in thrush territories even after removal of fruit. Another possibility is that the removal of fruit did reduce food levels below the level needed to meet energetic needs, but social constraints on territory structure, dictated by fall settlement spacing and maintained by agonistic interactions, prevented birds from adjusting territories to match food supply later in the season.     

Living on the edge: Fig tree phenology at the northern range limit of monoecious Ficus in China

Fig trees (Ficus) are a species-rich group of mainly tropical and subtropical plants that are of ecological importance because of the large numbers of vertebrates that utilise their figs for food. Factors limiting their distributions to warmer regions are still poorly understood, but are likely to include factors linked to their specialised pollination biology, because each Ficus species is dependent on one or a small number of host-specific fig wasps (Agaonidae) for pollination. Adult fig wasps are short-lived, but some species are capable of dispersing extremely long distances to pollinate their hosts. Close to its northern range limit we investigated the phenology of Ficus virens, the monoecious fig tree that reaches furthest north in China. Relatively few trees produced any figs, and very few retained figs throughout the winter. Despite this, new crops produced in spring were pollinated, with seasonally migrant pollinators from plants growing further south the most likely pollen vectors. An inability to initiate new crops at low temperatures may limit the distribution of monoecious fig trees to warmer areas.     

Tree species richness and density affect parasitoid diversity in cacao agroforestry

In Brazil, cacao is mostly planted beneath shade trees. The diversity of shade trees varies from monospecific to highly diverse canopies, characteristic of pristine Atlantic Forest. This study evaluates the relationships between family richness of Hymenoptera-Parasitica and Chrysidoidea, and tree species richness and density, the species richness of herbaceous understorey, and the area and age of the cacao agroforestry system. We sampled 16 cacao agroforestry systems, with canopy diversity ranging from one to 22 tree species per hectare, in three seasons: summer (March), winter (August) and spring (November). Parasitoids were sampled using eight Malaise-Townes traps per site. Tree species richness and density were enumerated within 1 ha at each site, and herbaceous plant species richness was calculated in eight 1 m² plots, within the hectare. The number of parasitoid families increased with tree species richness and density in spring and summer, but decreased in winter. Neither species richness of herbaceous plants nor area and age of the system affected parasitoid family richness. We suggest that the increase of parasitoid diversity with tree species richness and density in warmer seasons reflects increasing heterogeneity and availability of resources. The decrease in parasitoid family number with tree density in winter may be due to local impoverishment of resources, leading to parasitoid emigration to neighbouring forest remnants. This result implies that a higher diversity of shade trees will help to maintain high parasitoid levels and, in consequence, higher levels of natural enemies of cacao pests, particularly in the warmer seasons. This prediction is borne out in the experience of cacao producers. The proper management of shade tree diversity will play a vital role in maintaining the sustainability of cacao agroforestry production systems in the tropics and, concurrently, will maintain high biodiversity values in these locations.     

Nitrogen fertilization in citrus orchards

Summary The purpose of this review was to evaluate critically the results obtained in citrus nitrogen fertilization experiments in Israel and in other parts of the world, in order to increase our understanding of the processes involved and to improve the recommendations to growers. Mature citrus trees contain 1–2 kg N/tree, 30–60% of which is in the annual parts (leaves and fruits). 30g N is deposited annually in the tree skeleton. Based on these results and on a review of long-term fertilization experiments with citrus from various parts of the world, it was concluded that 200 kg N/ha applied annually is sufficient to sustain good citrus yields and tree development, about half of which is incorporated in the fruits and one-tenth deposited in the tree, the balance being made up by leaching and gaseous losses. Experiments with¹⁵N labeled fertilizer applications showed that the highest N-uptake rate occurred during fruit set and that in winter the uptake was very low. N reserves in the older tissues played an important part in the development of new leaves and flowers in the spring, when the uptake from the soil was still low. It was concluded that the nitrogen contained in the soil organic matter (2 Mg/ha) and in the mature trees (1 Mg/ha) plays an important part in the regulation of N supply to the growing parts of the tree. More N is derived from these parts with low N fertilization than with an abundant supply. The purpose of fertilization is to ensure proper development of the tree, not the current fruit yield. Contribution from the Agricultural Research Organization, The Volcani Center, Bet Dagan, Israel. No. 1770-E. 1986 series.     

Run,robber, run: parasitic acacia ants use speed and evasion to steal food from ant‐defended trees

Ants that are obligate plant associates protect their host against herbivores and aggressively defend the resources offered by the plant. Workers of Pseudomyrmex nigropilosus Emery (Hymenoptera: Formicidae), an acacia ant that parasitizes the mutualism by not defending the tree, are seen stealing food from other ant‐defended acacia trees. In the present study, hypotheses of evasion, chemical crypsis, chemical repellence and temporal activity patterns are tested in the field aiming to determine how P. nigropilosus enters other acacia trees, successfully circumventing the defence of the resident ants. When parasitic ants are stealing, resident ants are evaded by stopping walking, changing their walking direction or walking faster. Resident and parasitic workers have similar temporal activity patterns. Parasitic workers can walk 2.6‐fold faster compared with any of the three species of acacia‐ants from which they usually steal food. Behavioural assays suggest that P. nigropilosus do not have chemical repellence but that chemical crypsis may be involved in the evasion strategy. This last hypothesis needs to be explored further by chemical and olfactory analyses. The combination of speed and evasive reactions allows parasitic ants to access well‐defended acacia trees.     

Predator-induced defense makes Daphnia more vulnerable to parasites

Inducible defensive traits against herbivores or predators are widespread in plants and animals. Theory predicts that defended morphs have greater fitness in the presence of predators, but lower fitness than undefended morphs in the absence of predators. If such costs did not exist, then a constitutively defended morph would be favored by natural selection; yet, evidence for such costs has been elusive. Our current work reveals a significant cost to inducible defenses. Using the waterflea (Daphnia) model system, we show that induced defended morphs are significantly more vulnerable to infection by a virulent yeast parasite than undefended morphs. In two independent experiments, the proportion of successful infections and the number of parasite spores were higher among defended versus undefended Daphnia. Thus, by demonstrating a previously unknown and environmentally relevant cost to inducible defenses, this study enhances our understanding of adaptive phenotypic plasticity and its evolution.     

Fruit trees in a Malaysian rain forest

An inventory was made of 50 ha of primary lowland rain forest in Peninsular Malaysia, in which ca. 340,000 trees 1 cm dbh or larger were measured and identified to species. Out of a total plot tree flora of 820 species, 76 species are known to bear edible fruit. Especially diverse were the wild species of mango (Mangifera, Anacardiaceae, 12 spp.), mangosteen (Garcinia, Clusiaceae, 13 spp.), breadfruit (Artocarpus, Moraceae, 10 spp.) and rambutan (Nephelium, Sapindaceae, 5 spp.). Median population size for all species of fruit trees was 3.0 trees per ha and 0.2 adult trees per ha. Direct economic value of wild fruit trees was small; only one species has been very much collected and sold, Parkia speciosa (Fabaceae), amounting to less than US$20 per ha per year. The potential value of the species as genetic resources is very large: 24 species are cultivated, 38 edible species are congeneric with cultivated crops and at least 10 other species bear inedible fruit but are related to cultivated crops. We conclude that the Peninsular Malaysian rain forest is exceedingly rich in wild fruit trees, that these normally live at low densities, and that their principal economic value is as genetic resources.     

The spiny,thorny and prickly plants in the flora of Israel

To examine whether spininess evolved at random or differently in various life forms and plant organs, we characterized spiny, thorny and prickly organs in the entire wild flora of Israel (294 such species). Of the species, 63.3% defended their reproductive organs (the most‐defended organ) and 67.0% defended various non‐reproductive organs. Ninety‐three species defended both their reproductive organs and at least one other part; 48.3% defended their leaves and 36.4% their stems and branches. Spiny wings defended stems and branches only in herbaceous (annual or perennial) species. There were clear differences between the life forms. Annuals and perennial herbs defended mostly their reproductive organs (95.7 and 83.0%, respectively), dwarf shrubs defended mostly their leaves (54.2%) and shrubs and trees mostly their branches (89.7 and 76.2%, respectively). Trees do not defend their reproductive organs by associated sharp appendages. The differences in defence on various organs among different life forms may influence the results of meta‐analysis studies of the optimal defence allocation if such differences are not taken into account. We noted spine, thorn and prickle colours for 167 species with yellow, red, orange and white being the dominant, supporting hypotheses about spines being visually aposematic. © 2012 The Linnean Society of London, Botanical Journal of the Linnean Society, 2012, 168 , 344–352.     

Feeding ecology of the northern Ryukyu fruit bat, Pteropus dasymallus dasymallus, in a warm-temperate region

The warm-temperate fruit bat, Pteropus dasymallus dasymallus consumed at least 17 species of fruits, five of flowers, nine of leaves, one of bark and eight of insects. Soft fruits formed the bulk of its diet. Ficus eaten by the bat fruited asynchronously among individuals of the same species. In these species, the ratios of trees bearing ripe fruit to all trees cxamined each month were very low except for F. erecta. On the other hand, some plant species showed synchronous fruit production over a short period. Both types of plants supply fruits in every season. Seasonal dietary shifts and food choice were evident, and flowers, leaves or insects formed a small but nutritionally important component of the diet of the bat. The frequency of mastication was 124–155 per one pellet produced within a few minutes. The bat extracted and swallowed 61 82% ofthe fruits' wet weight and 58–73% of the insects' weight. The swallowed juice passed through the digestive systems in only 34 min on average. The bat ingested 0.5 times its body weight in figs per day. It is probablc that such a low food intake is adapted for the seasonal changes of food availability in the warm temperate region.     

Inducible defenses,competition and shared predation in planktonic food chains

Ecologists have long debated the role of predation in mediating the coexistence of prey species. Theory has mainly taken a bitrophic perspective that excludes the effects of inducible defenses at different trophic levels. However, inducible defenses could either limit or enhance the effects of predation on coexistence, by means of effects on bottom-up control and population stability. Our aim was to investigate how inducible defenses at different trophic levels affect the possibilities for predator-mediated coexistence, as opposed to competitive exclusion, in replicated experimental plankton communities. In particular, we analyzed how the presence or absence of inducible defenses in algal basal prey affected the outcome of competition between an inducible defended and an undefended herbivore, in the presence or absence of a carnivore. We found the undefended herbivore to be a superior competitor in the absence of predation. This outcome was reversed in the presence of a shared carnivore: populations of the undefended herbivore then strongly declined. The extent of this population decline differed between food webs based on undefended as opposed to inducible defended algal prey. In the former the undefended herbivore became undetectable for most of the duration of the experiment. In the latter the undefended herbivore also crashed to low densities, but it could still be detected during most of the experiment. In food webs based on inducible defended algae, the carnivore failed to reach high densities and exerted weaker top-down control on the two competing herbivores. We conclude that the inducible defense in one of our two competing herbivores allowed the outcome of competition to be reversed when a shared carnivore was added. Inducible defenses in algae did not change this outcome, but they significantly delayed extinction of the undefended herbivore. Predation itself did not promote coexistence in these experimental plankton communities.     

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.     

Foraging behaviour of the middle spotted woodpecker Dendrocopos medius in Sweden

During winter and spring the oak Quercus robur , was the tree species most utilized by middle spoiled woodpeckers. In March, saptrees, mainly maples Acer platanoides , were preferred for a short period. In winter the birds foraged in the crowns of oaks but in spring they preferred lower stem parts. Dead branches were utilized more in winter than in spring. The birds mostly used a gleaning and probing technique, which may render the species more senstitive to severe weather conditions than other woodpecker species. Arthropods collected from trees were mostly spiders, beetles, thrips or springtails. The nestlings were mainly fed on scale insects and larvae of moths and sawflies. The oak habitat specialization is believed to be caused by competition for food with other gleaning forest birds. Food shortage might possibly occur during periods of bad weather, causing increased mortality.