Plant-Animal Interactions: An Evolutionary Approach (3)

This will be my last post about the book. You can read my previous posts about the book here and here.

As I have already mentioned, I really liked this book. Below I have covered some of the parts of the book which I have not yet talked about here on the blog, and in particular I’ve included stuff about how plants and animals cooperate with each other. I have of course had to leave a lot of stuff out.

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“The lack of mobility in plants creates a physical obstacle in the dispersal of their genes. In a majority of all plants, this obstacle has been alleviated through the formation of mutualisms with animals that transport pollen grains between stigmas and also disperse seeds. In the case of pollination, the goal for the plant is to receive pollen on its stigma and to have pollen picked up and deposited on conspecific stigmas of other plants. The animal most commonly seeks a food reward. It is important to appreciate that mutualisms such as these represent reciprocal exploitation with an underlying evolutionary conflict. Selection in mutualisms favours selfish behaviour […] One manifestation of such selection […] is the widespread phenomenon of plant species that no longer reward pollinators but instead attract visitors by deception. […] Non-rewarding plants species constitute a substantial portion of all angiosperms, especially among orchids, but they are mostly minor components of the plant community in which they grow. […] Likewise, many flower-visitors (if not most) do not contribute to pollination but do remove floral resources such as nectar and pollen. […] A fair number of plants mimic not flowers but rather pollinator mates or oviposition sites. Flowers of the well-studied European fly orchids (Ophrys) and caladeniine Australian hammer orchids provide visual, olfactory and tactile cues mistaken by naïve wasp males for conspecific females (Stowe 1988), and pollination happens as males attempt copulation with the flowers.” [This sentence made me laugh!]

“pollination mutualisms evolve amid simultaneous antagonistic interactions; the plant is under selection to maximize the net fitness of attracting potentil mutualists at the lowest net cost while minimizing the detrimental effects of non-mutualists or low-quality mutualists. This tradeoff does not exist in antagonistic interactions […] Floral traits are likely to be as much the result of selection for avoidance of some animals as for attraction of others. […] The vast majority of all extant pollination mutualisms […] involve flowering plants, which dominate most biota on earth today.”

“Given that the benefit to plants of animals as pollen vectors is transport across longer distances, it is not surprising that the three extant groups of animals that have evolved flight – insects, birds and bats – contain a very large proportion of all pollinators. Among the insects, flower-visiting species are particularly frequent within the large orders Hymenoptera (bees and wasps), Lepidoptera (moths and butterflies), Diptera (flies) and Coleoptera (bettles). […] The Lepidoptera alone, whose coiling tongues make them flower specialists and effective consumers of nectar, constitute 11% of all described species on Earth […] Among birds, six phylogenetically independent groups have diversified as flower-visitors and often as pollinators […] Together these groups constitute over 10% of all recognized bird species. […] Flowers offer an extraordinary range of shapes, colours and scents, reflecting high rates of evolutionary change in these traits. […] Almost any flower part or even adjacent leaves are modified for the purpose of attracting pollinators. There is arguably more plasticity in these secondary reproductive traits in plants than in any other organismal groups, with the possible exception of birds.”

“Specificity among visitors is a necessity for effective pollination; if animals visit flowers of different species indiscriminately, heterospecific pollen transfer will result, which reduces the probability of pollen reaching a conspecific stigma […] The number of plant species visited varies greatly among flower-visiting species. […] Individual visitors often tend to specialize on a subset of potential flowers during any one foraging bout; in bees perhaps 90% of all visits may be made to a given species, with occasional visits to other species. This short-term specialization is referred to as floral constancy. The dominant flower may vary among simultaneously foraging conspecifics, and within individual visitors on successive foraging bouts. Reasons for such short-term selectivity have been explored in insects, and focus on the effects of foraging rate as a result of memory constraints. Insects must learn by trial and error how to effectively access a reward such as nectar in more complex flowers, as the rewards are concealed and most quickly accessed using a particular approach. Minimum handling time may be approached only after as many as 100 visits to a given zygomorphic flower […] visitors may be unable to keep more than one sensorimotor protocol in active memory, thus making it a superior strategy to focus on one food source at a time […] Specialization is often not in the evolutionary interest of a flower-visiting animal, as its ultimate interest is to optimize the reward harvesting rate over time. A foraging pattern that maximizes the harvesting rate of commodities such as nectar and pollen can include two or more coexisting plant species, especially if their floral structure is fairly similar so that the visitor can use a single visit behaviour protocol. […] The vast majority of all plants are pollinated by two or more species”

“With the […] exception of ants […], invertebrates play only an anecdotal role as seed-dispersers […] All major lineages of vertebrates take part in fruit consumption and seed dispersal, but their importance as dispersal agents is very unequal. Birds and mammals are the only or main dispersers of the vast majority of vertebrate-dispersed plants […] About 36% of 135 extant families of terrestrial birds, and 20% of 107 families of non-marine mammals, are partly or predominately frugivorous […] Fruit consumption by vertebrate dispersers […] has selected for fruit traits that enhance detectability by frugivores […] Although exceptions abound, fruits that are green or otherwise dull-coloured when ripe tends to be associated with seed dispersal by mammals, whereas fruits dispersed by birds tend to be brightly pigmented. The partial dichotomy between ‘bright’ and ‘dull’ ripe fruits has probably been selected for by the contrasting sensory capacities of birds and mammals […] Size is an important attribute of fruits, because it sets limits to ingestion by relatively small-sized dispersers that swallow them whole, like birds. […] Fruits eaten by mammals tend to be larger than those eaten by birds […] Fruit pulp is the reward offered by plants to dispersers, and its nutritional value is a critical element in the plant-disperser interaction. Compared to other biological materials, fruit pulp is characterized, on average, by high water and carbohydrate content, and low protein and lipid content. […] the occurence of secondary metabolites within ripe pulp presumably represents a tradeoff with respect to defence from damaging agents and palatability for dispersers […] A number of studies provide unequivocal support for the ‘palatability-defence tradeoff hypothesis’. […] increased frugivory is quite often associated with increased intestinal length, as an adaptive response for increasing intestinal absorption of the water-diluted nutrients in fruit juice. […] Most fruits are very deficient in nitrogen, which perhaps represents the most important nutritional constraint that frugivorous animals must cope with. Regular ingestion of small amounts of animal food seems to be the commonest way of complementing the poor protein intake associated with frugivory.”

“Abundance of fruit varies markedly among years and seasons, and within as well as between habitats, which generally leads to patchy and unpredictable distributions in time and space […] A distinct suite of behavioural and physiological traits allow frugivores to withstand or escape from temporary situations of fruit scarcity and efficiently locate unpredictable fruit sources. Seasonal migration and habitat shifts are the two most common generalized responses of frugivores to fluctuations in fruit availability. […] Plant-vertebrate dispersal systems are characterized not only by the absence of obligate partnershipts, but also by weak mutual dependence between species of plants and animals, and by the prevalence of unspecific relationships. […] the general picture is one of loose interdependence between species of plants and species of dispersers. […] pollen and seed dispersal by animals are fundamentally dissimilar […], and their differences have manifold evolutionary implications. The two most important distinctions are (i) that a definite target exists for dispersing pollen grains (the conspecific stigma) but not for dispersing seeds; and (ii) that the plant can control pollinators movements by providing incentives at the target site (nectar, pollen), but there are no similar incentives for seed dispersers to drop seeds in appropriate places. These differences are best framed in terms of the departure-related versus arrival-related advantages of dispersal [You can say that seed-dispersal systems work on the basis of ‘advance payment’ alone, whereas pollen dispersal mechanisms also include ‘payment upon delivery’ aspects].”

Finally, ants! Ants are awesome…

“Ants are one of the most abundant, diverse and ecologically dominant animal groups in the world. They make up from 10 to 15% of the entire animal biomass in many habitats, and in the Amazonian rainforest, for example, one hectare of soil may contain 8 million individuals. The impact of ants on the terrestrial environment is correspondingly great. In most habitats they are among the leading predators of other insects and small invertebrates, and in some environments they are the principal herbivores and seed predators. Ants can alter their physical environment profoundly, moving more soil than earthworms, and being major channellers of energy and cyclers of nutrients. […] It is probably fair to say that no other animal group interacts with plants in such diverse ways. Indeed, the fact that ants are the only specific taxa mentioned in the chapter headings of this book reflects their ecological importance in the lives of most plant species. Ants can protect plants directly from herbivores or from competition with other plants. They can also affect plant-community composition and dynamics by selective weeding or ‘gardening’, altering nutrient availability, pollinating flowers, or dispersing and harvesting seeds. Plants provide ants with food and shelter […]. Some relationships between ants and plants appear to be highly coevolved mutualisms and it is these interactions that have received the most study. But the majority of ant and plant species interact in more generalized ways, often through the influence of ants on the chemical and physical properties of soil. […] The oldest ant species, Sphecomyrma freyi, has been dated from amber to be about 80 million years old. [….] there is evidence that ants have been both remarkably diverse and ecologically successful for at least 50 million years”

“Cultivation of fungus by attine ants originated about 50 million years ago. The relationship between the higher attine ants and the symbiotic fungus they cultivate is obligate. Foundress queens propagate the fungus clonally by carrying a pellet of fungus in their mouths during their nuptial flight to establish new colonies. […] The relationship between the attines and their fungus has been termed an ‘unholy alliance’ because it combines the ants’ ability to circumvent plants’ anti-fungal defences with the ability of the fungus to subvert plants’ anti-insect defences. The ants benefit because the fungus breaks down plant tissue such as cellulose, starch and xylan, and possibly detoxifies insecticidal plant compounds. The fungus thus enable them to make use of plant material that would otherwise be unavailable and allows the ants to be truly polyphagous in the midst of diverse flora. […] the relationship between the ants and the fungus has recently been found to be a triumvirate, with evidence that an antibiotic-producing bacterium is an important component of the symbiosis. […] fungus gardens are particularly prone to infection by a group of closely related, highly specialized parasites in the fungal genus Escovopsis. […] Escovopsis is found in gardens of virtually all species of fungus-growing ants, but not elsewhere. The parasite is usually found at low levels, but if the health of the garden is compromised it can quickly take over and destroy the fungal crop. In healthy gardens, Currie et al. (1999) have shown that the fungus is kept in check by specific antibiotics produced by Streptomyces bacteria living on the bodies of the ants […] The bacterium can also promote the growth of the cultivated fungi. The position of the bacterium on the ant integument is genus-specific, indicating that the association with the ants is both highly evolved and of ancient origin […] Attine symbiosis appears to be a coevolutionary arms race between the garden parasite Escovopsis on the one hand, and the tripartite association of the actinomycete, the ant hosts and the fungus on the other. The relationship raises the interesting question of how the attine antibiotics have remained effective against the fungus-garden pathogens for such a long time, given that resistance to antibiotics is a well known problem in human and other populations.”

“The coevolution of ants and plants involving systems of rewards and services has resulted in a variety of elaborate and complex mutualistic interactions collectively known as ant-guard systems. Here the rewards are extra-floral nectar, specialized food bodies and nest sites, while the service is the protection of the plants from herbivory. […] Plant structures known as domatia are developmentally determined and appear to be specific adaptions for ant occupation. They are often formed by the hypertrophy of internal tissue at particular locations in the plant, creating internal cavities attractive to ants […] the plant species that bear them are known as myrmecophytes. […] Some myrmecophytes are actually ‘fed’ by the ants they house. Experiments have shown that two genera in the family Rubiaceae […] absorb nutrients from the wastes of the Iridomyrmex colonies they house in tunnels inside large tubers […] A variety of field studies have shown there is strong competition among ants for dormatia […] Ant-guard systems involving extra-floral nectaries are often complicated by the presence of Homoptera or lepidopteran larvae that secrete nectar-like fluids collectively known as honeydew. In such situations, the ants have a choice of food and the outcome of these three-way interactions between plants, ants and herbivores appears to be extremely variable. The Homoptera include herbivores such as aphids, leafhoppers, scale insects and coccids. Each animal is armed with a proboscis that penetrates plant vascular tissue, tapping into the nutrient supply. With little apparent effort, the sap enters the front end of the homopteran gut, later appearing at the back end as droplets, somewhat depleted in quality but still containing many nutrients, where it is ejected as honeydew. Many ant species harvest the honeydew and, in return, protect the homopterans from predators and parasites […] As a result, ant activity can increase levels of herbivory as well as other forms of damage […] Ant interactions with plant species that produce extra-floral nectaries, food bodies and domatia have evolved both in the presence of homopterans and lepidopteran larvae and the ant behaviour that protects them. For example, homopterans of various kinds are routinely maintained within domatia and they frequently feed on plants that bear extra-floral nectaries. This leads to the situation where plants are providing rewards for ant-guards that attack some of the plant’s enemies but protect others. A solution to this apparent conflict of interest was first proposed by Janzen (1979) who suggested that the presence of homopterans was part of the cost of the ant-guard system […] The evoluation of extra-floral nectaries has itself been viewed as a defence against homopteran attack, weaning ants away from the herbivores […] Homopterans are common herbivores and have been around for a very long time; thus, given their ubiquity, selection for extra-floral nectaries may have resulted in the plants exerting greater control over the ant-guards, provided ants preferred nectar to honeydew.”