ZOOLOGY Principles of Ecology Prey Predator and Plant Herbivore

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Paper No. : 12 Principles of Ecology Module : 16 Prey predator and Plant herbivore interactions: Part II

Development Team

Principal Investigator: Prof. Neeta Sehgal Head, Department of Zoology, University of Delhi

Co-Principal Investigator: Prof. D.K. Singh Department of Zoology, University of Delhi

Paper Coordinator: Prof. D.K. Singh Department of Zoology, University of Delhi

Content Writer: Dr. Haren Ram Chiary and Dr. Kapinder Kirori Mal College, University of Delhi

Content Reviewer: Prof. K.S. Rao Department of Botany, University of Delhi

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Description of Module

Subject Name ZOOLOGY

Paper Name Zool 012 Principles of Ecology

Module Name/Title Species interaction

Module Id M16 Prey predator and Plant herbivore interaction: Part II

Keywords Defoliation, Mimicry, Structural defense, Predation Satiation, Chemical defense, Herbivore countermeasures

Contents 1. Learning objectives 2. Introduction 3. Predation on plants 4. Effects on plant fitness 5. Effects on Herbivore fitness 6. Plant defense system a. Mimicry b. Structural defense c. Predator Satiation d. Chemical defense 7. Herbivore Countermeasures 8. Summary

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

1. Learning Outcomes

After studying this module, you shall be able to

 Describes the predation on plants  Understand the effect of herbivore on plant fitness and vice-versa.  Illustrate the mechanisms adopted by plant as defense mechanisms including mimicry, structural, chemical features and predator satiation.  Define the measures adopted by herbivores to counteract the defense mechanisms of plants.

2. Introduction

The act of eating plant is called herbivory. Above or below the ground, the herbivory can occur in both. Herbivores are the living organisms that consume whole plant or any part of the plant above the ground (soil) such as flowers, stems, fruits, leaves and any plant part lying below the ground (soil) such as tubers or roots (fig.1). The plant species are the host species (or preys) for the herbivores acting as predators, and the interaction between them creates an important ecological association called plant-herbivore system. The plant-herbivore interactions play critical role in the ecology of any habitat, influencing individual plant growth and development and plant communities. The diversity of plants is enormous reflecting the broad diversity of vertebrates and invertebrate herbivores that feeds on them. Wide ranges of feeding opportunities are offered by the individual plant species and the dependent herbivore organisms developed many adaptations in form of specialized features and feeding strategies to consume their food source or plants. As an example, the adaptation of specialized features includes behavioural changes and modified mouthparts that allow herbivores to consume on plant species. In order to utilize plants as their food source, the predators have to overcome the specialized features plants have adapted against their consumers. This type of interaction between plants and herbivores developed an arms race between them and lead to establishment of a strong relationship between them. The herbivores may range from organisms depending on particular plant structures as food source to organisms dependent on particular plant species or groups. Animal which are specialized to feed on certain plant group or species as their food source for their growth and development are called as “plant host specific” and the specialization is called as plant host specificity. Thus, for the management of the community or land, deep understanding about the plant- herbivore relationship is very important. From any given habitat, the exclusion of particular plant group or species may leads to the loss of many herbivores. The plant-herbivore interactions have substantial influence on the health of the habitat, the diversity and structure 3

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

of the soil and plant communities. This type of predation may have positive impact on the communities or species such as herbivory up to a certain level increases the production and nutrient uptake by the plants as the feeding may remove aged leaves and roots triggering the growth of young shoots and roots that are more efficient in supporting the growth and developmental processes. The herbivore organisms while eating the plants cause parts of the plants to fall and their own faeces that may contribute to nutrient pool and litter in soil. The consumption of plants favours young foliage to fall down on ground contributing high quality of leaf litter with higher nutrient value to the soil. Trimming of the plants by the herbivores may cause seeds to fall down that are transported by the ants to their nests in the soil. The water and nutrient rich soil of ant’s nests offers favourable area for the successful seedling growth of plants. Moreover, plants pruned by the herbivores allow light to reach the ground and stimulate the growth of seeds by providing favourable surroundings. Furthermore, some plant-herbivore relationships offer protection to plants as shown by ant-acacia association. Additionally, primary (initial) herbivory triggers the release of certain chemicals or secondary metabolites from the pruned plant areas that attracts parasitoids and predators to control further herbivory.

Figure 1: An example of Plant-herbivore system: Deer grazing on plants

3. Predation on plants

Both, consumption of seeds and fruits and defoliation are the two major types of herbivory forms on the plants. These two forms of predation by herbivores on plants cause different results.

The destruction of external structures of plants is called defoliation. The plants tissues can be roots, leafs, sap, bark and stem destructed by the predators. Some predators do not kill the plants or directly consume the tissue, but, depends on the plant juices whereas some predators kill plants or destruct the parts of the plant by directly consuming the tissues. Below is a list of different types of feeding strategies for plant eaters: Palynivore- pollen eaters (e.g. some 4

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

insects); Foliovores- leaf eaters (e.g. koalas); Frugivores- fruit eaters (e.g. flying foxes); Nectivores- nectar eaters (e.g. hummingbirds); Graminivore- grass eaters (e.g. zebra) and Granivores- grain eaters (e.g. some rodents) etc.

Some herbivores (predators) kill the plant by grazing the seeds. However, if the grazer consumes only parts of the plants than the continuation and amount of grazing will decide the survival rate of consumed plant. Defoliation always has adverse effects, even if the plant regenerates and persists long. The biomass of the plants is reduced by grazing activity. In 1977, Harper suggested that roots and foliage pruning reduces the competitive ability of the plants, its vigour and fitness.

Predation can be advantageous to plants, where palpable fruits containing seeds are consumed by the fruit-eating herbivores and the seeds are carried to their guts from where they enter the process of seed dispersal. However, there are cases where seed predation has no impact; on the other hand, there are cases where seed predation can prevent the rate of increase in population or colonization of plants.

4. Effects on plant fitness

Herbivory causes destruction of plant tissues like stem, leaves, roots, flowers, sap and fruits which in turn effect the survival rate and overall fitness of the plant without killing the plant. Roots pruning and loss of foliage reduces the plant biomass and decreases the fitness, reproductive and competitive ability and vigour of the plant. Moreover, at the most vulnerable stage of plant growth and development i.e. its juvenile stage, herbivory produces strong adverse effects. On contrary to mature leaves which are net exporters of nutrients, the young leaves import nutrients from roots and other reservoirs (plant tissues). Rabbits, deer, larvae of gypsy moth, and sawfly are the common grazing herbivores that depend on more nutritious and palpable leaves (fig.2). They reject eating mature and older leaves being less palpable, high in secondary compounds such as tannins and complex chemical structures like lignin.

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Figure 2: A grazing herbivores- Black Rhino

In response to herbivory mediated defoliation, the plant support regeneration and new growth by the import of nutrients from reservoirs like roots and other tissues that otherwise is planned to used by the plants for its own growth and development. A costly response of plants to defoliation is the stimulation of chemical defenses. The plant physiology gets altered on severe defoliation by the herbivores followed by subsequent re-growth of the lost parts. Consumption of leaves to a critical level alter the levels of hormonal growth regulators which in turn control the bud dormancy, thus, resulting into late formation of buds for next year’s growth. The re-foliation at the expense of reserve nutrients adversely affects the overall fitness of plant and they become more susceptible to the attacks of insects and diseases. Moreover, the plant has no available resources for reproduction.

Aphids and other plant herbivores do not directly consume the tissues rather tap plant juices and called as sap suckers. These harbivores reduces the biomass and growth rate of plants. Moderate grazing acts as advantageous process in some group of plants, grasses and in forest canopy. It has a stimulating impact on plant growth thereby increases the production of biomass but at the expense of reserve nutrients and vigour.

Grazing may benefit from and are well adapted to; moderate grazing that increases the biomass production. Owen and Weigert (1981) suggested that even at the cost of reduced sexual reproduction arte, the fitness of some grasses can be maintained only under the pressure of grazing.

5. Effects on Herbivore fitness

Herbivory is a two-edged sword, where both the interacting organisms have pronounced effects on each other’s fitness. Herbivores adversely, sometimes advantageously, affect the

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

plants; similarly plants have prominent effects on the fitness of their predators. The primary production of herbivores is related to its consumption, biomass and production.

Thus, plant affects the fitness and population dynamics of herbivores to greater extent in comparison to the effects of herbivores on population dynamics of plants.

It’s not the quality but the quantity of food resources availability that cats as a critical viewpoint for herbivores. Although enough plant biomass is available for the predation yet herbivores requires nitrogen rich high-quality foliage as specialized digestive process is essential to breakdown plant cellulose and convert the digested parts of plants into animal tissues. Without that, full stomach herbivore can also starve to death.

Green, soft and young storage organs like seeds, tubers and roots are the high quality foods utilized by the herbivores. Adding to the problem of quality of available food resources, the herbivores may experience difficulty in overcoming the defense mechanisms adopted by the plants.

Plants as a defense strategy make their tissues unavailable, unpalpable, hardly digestible or even toxic.

Secondary metabolites are the plant substances that adversely affect the reproductive rate of herbivores. Ladino clover and alfalfa are the legumes with high concentration of iso- flavanoids. These iso-flavanoids are the secondary compounds in plants that mimic estrogenic hormones such as progesterone. Thus, when grazing herbivores consume these iso-flavanoids, a hormonal imbalance is induced in them resulting into reduced lactation, difficult labor and infertility.

6. Plant defenses system

In the plant-herbivore association, the plants are at disadvantage as they are immobile/ or fixed in place. Thus, certain modes of defense are adopted by plants to counteract herbivore attacks. These defense mechanisms range from mimicry and chemical methods to structural features.

a. Mimicry In the Plant Kingdom, plants in response of food search by herbivores have stimulated an evolutionary process resulting into mimicry. In 1975, L.E Gilbert evidenced mimicry as the mode of defense in a plant, Passiflora (the passionflower) against the predatory butterfly called Heliconius (fig.3). In the New World tropics, the passionflower plant comprised of nearly about 350 species varying in the shape of leaves due to wide range of intra- and interspecific differences.

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Figure 3: Passionflower and (left) Passionflower butterfly

Each species of passionflower butterfly is dependent on a limited group of food plants (Passiflora species). The Heliconius butterflies are highly host specific and around 45 vspecies of this passionflower butterflies are dependent on passionflower sp. as a source of larval food and egg-laying site. The passionflower plant species vary in the leaf shapes within a particular habitat. The passionflower butterflies are visually very sophisticated and they locate the position of the passionflower plants on which they lay the eggs to confirm that particular plant on repeated visits. But the passionflower plants evolved leaf forms as a response against the visual selection of butterfly, disabling them to relocate the plants. Under selection pressure, leaf forms of passionflower converge with other tropical plants that are inedible for Heliconius butterflies. The convergence is so strong that the passionflower species are taxonomically named after their resembling genera of other plant species.

Furthermore, Passiflora auriculata and Passiflora cyanea are the Passiflora species that exhibit egg mimicry. These passionflower plant species evolved outgrowths near the leaf bases that mimic the shape, size and color of passionflower butterfly eggs at their hatching stage. Based on the concept that female Heliconius butterflies reject shoots that already have larvae or eggs of other females the Passiflora species achieves protection by egg mimicry (fig.4).

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Figure 4: Passion-flower leaf showing Egg mimicry

b. Structural defenses Plants adopted different structural features as a method of defense to make herbivore predation difficult. It’s a least costly defense method which includes spines, tough leaves, thorns and epidermal hairs on leaves to trap insects and discourage browsing (fig.5). Under predatory pressure and in order to discourage seed-eating herbivores, many plants produce seeds that have hard seed coats and are thick. However, some plants exploit seed predation by herbivores as a seed dispersal mechanism.

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Figure 5: (a-c) structural defense (spinescence) such as thorns, spines and prickles, (d) trichomes on plants and (e) sclerophyllous leaves.

In 1986, Cooper and Smith performed experiments to understand the role of structural defences in plants against herbivore predation. Their experiment demonstrated the defensive effectiveness of apparent structures features against grazing herbivores. Three large browsing mammalian herbivores, namely kudu, impala and Boer goat are used to investigate the effects of plant spinescence on the selected herbivore’s feeding habits (fig.6). In South Africa, the Northern Transvael bushveldlt associated Nylsvley Nature Reserve was the study area for the experiment. The experiment demonstrated that the structural features of woody plants in the study area increases the handling time and restricts the bite size of grazing herbivores. The structural features like thorns, prickles and spines restrict the loss of foliage by the grazing activity of herbivores. Additionally, the grazing herbivores are adversely affected and incur scar and scratches in the oesophagus, oesophageal mucosa and buccal mucosa.

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Figure 6: Kudu grazing in South Africa, (right) Impala grazing in the National Park of Africa

c. Predator Satiation

Both plants and animals provide defense against predation by regulating the reproduction time via physiological mechanisms, enabling the production of maximum number of offspring’s in one short period of time. Predators achieve satiation on abundance of prey population. In plants, the major strategy against herbivores is called Predator Satiation, more commonly called as predation saturation, especially in those plant species that do not have chemical defense mechanisms. There are four types of approaches used by the plants against predation by herbivores: i. First approach is the distribution of seeds in such a manner that the whole seed crop is not equally susceptible to predation by seed herbivores. Seed predators concentrate on parent plants and its nearby spread seed crops but missed the seeds spread to distant areas because of unprofitability and search image. ii. Second approach adopted by plants is to shorten the time of seed availability. Before germination, if all the matured seeds are available at one time, the seed predator becomes incapable of exploiting entire seed crop. iii. Third approach is periodical production of seed crops rather than annual. Plants like oaks adopted this strategy which has longer time between successive seed crops discouraging support to large population of seed dependent predators between successive seed crops. Thus, causes reduction in the predator density to exploit next seed crops. iv. Internal physiological constraints and weather events bring synchronization of seed production that causes periodical production of seed crops. Synchronization across species achieves predator satiation, which is the forth type of approach used by the 11

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

plant species as a defense mechanism. If two plant species sharing same predators at the fruiting season have same timing of the seed crop than predatory pressure on both plant species is shared and reduced, on the other hand assuring predator satiation also.

d. Chemical defenses

In plants, the first line of defense against predation is the chemical defense based on the secondary compounds accumulation within the cells or epidermal glands. The secondary products are the by-products of primary metabolites involved in the plant metabolic processes. These secondary metabolites ranges from phenolics to alkaloids, steroidal, terpenes, mustard oil glycosides, resins, tannins and cyanogenic. Alkaloids are the amino acid derivatives; phenolics are ubiquitous and are the by-product of amino acid metabolism. Storage and production of chemical metabolites are costly to plants. There are two types of chemical defense mechanisms against herbivory:

a. One type of resistance approach includes storage and production of metabolites released at wound site and act as toxins against bacteria, nematodes and fungi. b. The other type involves inhibitors acting as repellents, direct poison, warning odors or attractant (decoy) before attack by fungi or animal feeding.

The consumption of foliage and seeds is discouraged by cardiac gylcosides and tannins which impart bitter taste to plant tissues. Saponins, phenolic terpenes and other metabolites are toxic to herbivores causing illness or even death.

The chemical defense in plants is often offer by the mutualistic relationship between fungi and plants. For instance, Acremonium ceonophialum, an endophytic fungus share a mulutaistic association with plant Festuca arundinacea (fig.7). The fungus grows and may even extend through intercellular space, thus, derives nourishment from the fluid of intercellular space. In turn, the fungus provides protection to tall fescue plant against large herbivores like horse and cattle by producing toxins causing reproduction failure, poor weight gain and heat intolerance in the grazing animals.

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Figure 7: Festuca arundinacea plant, infestation of Acremonium ceonophialum fungus growth.

The nature of plants defines the mode of defense. In 1975, Feeney distributed plants into two major groups: apparent and unapparent whereas Rhodes and Cates divided plants into two types: predictable and available; and unpredictable and unavailable. The two sets of terms are synonymous. a. Apparent plants: These are the type of plants which are easy to locate by the herbivores and are easily available for herbivory, thus have synonyms like available and predictable plants. These are large and woody and usually long lived plants. They posses dosage dependent or quantitative type of defense. Resins and tannins are the major type of secondary metabolites involved in this type of defense mechanism and are localised in seeds, bark or near the leaf surfaces. They offer low palpability and reduce the rate assimilation, ability to digest by forming indigestible complexes with proteins in leaf. But, this type of defense provides a slow response against predation. b. Unapparent plants: These plants are usually perennials and annuals, short-lived and dispersed in time and space. Unlike quantitative defense in apparent plants, unapparent plants offer qualitative defense. Alkaloids and cardiac glycosides are the secondary metabolites which provide highly toxic defense against grazing which in non-adapted insects causes disruption in development or interfere with metabolic process of animals. Such defense responds quickly and cost effective for plants even at low concentrations. However, there is no absolute distinction between quantitative and qualitative defense or unapparency and apparency.

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

7. Herbivore countermeasures

Many external structures are present in plants such as stems, fruits, leaves, flower parts, seeds, and roots. The forms of each of these external structures differ in different plant species. However, access to these external structures is possible attributing to the certain characteristics of the herbivores. These characteristics of herbivores include modified legs that help in them in digging and enable them for the consumption of roots. Appendages like spines, claws or suckers help herbivores to grip onto the inverted or vertical surfaces of plants and wings offers ability to reach highest parts of the plants. Additionally, chewing mouthparts as cutting tools (e.g. in beetles), tube-like mouthparts as piercing tools (e.g. in wasp ovipositor) and saw-like tools possessed by sawfly ovipositor are the characteristics of the herbivores to gain access to internal structures.

Lignin and cellulose are the complex compounds essential for the plants to maintain their support and physical structure. These complex compounds are insoluble in water, difficult to digest and tough. To gain access to these tough and chemical plant tissues, several feeding strategies are employed by the herbivores including chewing mouthparts, tube-like mouthparts etc. Other strategies employed by the herbivores to avoid and/or eat tough parts of the plants include:

a. Alliance formation: in order to consume the tough part of the plants, some insects like Ambrosia beetles, form alliances with fungi and bacteria that can digest the complex chemical structures (fig.8). The Ambrosia beetles consume the digested tough parts by allocate fungi that digest the complex structure of plants into liquefy material.

Figure 8: Ambrosia beetles form alliances with fungi

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

b. Chewing mouthparts: Butterflies, locusts, larvae of moths and beetles are the most prolific chewers. Leaf chewers wedge through leaves attributing to their mouthparts. The leaf chewer includes katydids, stick-insects, locusts, sawflies and grasshoppers. Some organisms collect fragment of leafs to feed their young ones or to construct their nests such as wasps, ants, leaf-cutter bees, and termites (fig.9).

Figure 9: Leaf chewers c. Attack soft internal parts: Some herbivores such as miners avoid consuming the tough parts of the plants rather take the soft internal tissues. Sawflies, moths, wasps and larvae of some flies and insects are the common miners that eat between plant cell layers. d. Mining: the entire leaf is consumed by the leaf miners rejecting the outer protective layers of the leaf and veins. Appearance of blisters, blotches and tunnels on the plant leaves depicts mining activity (fig.10).

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Figure 10: Leaf Mining

e. Rostrum or tube-like mouthparts: Sap suckers like bugs (fig.11) have rostrum or tube- like mouthparts to pierce through the tough tissues and suck the internal juices.

Figure 11: Sap-sucking Bug

f. Nectar feeding mouthparts: Nectar feeding mouthparts for sucking, sponging and lapping on nectar are adopted by nectar feeding specialists such as insects including moths, wasps, flies, butterflies, bees and beetles, and vertebrates like honey possums and lorikeets (fig.12).

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

Figure 12: Honey possum licking nectar

All animal posses a detoxifying mechanism against the chemical defense of secondary metabolites, called as mixed function oxidase (MFO). MFO is an enzyme that metabolizes the potential toxin substances or foreign compounds. Liver of the vertebrates, Malpighian tubules, fat bodies and gut of the insects are the sites which posses MFO activity. Lipophilic or fat rich foreign substances are converted by the activity of MFO into water soluble molecules via hydrolysis, reduction and oxidation, these water soluble molecules can now be excreted out from the body.

8. Summary

The predator-prey system depicts the association of interacting predators with prey population. Prey-predation relationship at one trophic level may affect the prey-predation relationship at the next trophic level. The predator-prey system involves herbivory: a plant- herbivore system and carnivory: herbivore-carnivore system. Plant predation includes both consumption of fruits and seeds and defoliation by grazing animals. The act of eating plant is called herbivory. Herbivores are the living organisms that consume whole plant or any part of the plant. The plant species are the host species (or preys) for the herbivores acting as predators, and the interaction between them creates an important ecological association called plant-herbivore system. The diversity of plants is enormous reflecting the broad diversity of vertebrates and invertebrate herbivores that feeds on them. Both, consumption of seeds and fruits and defoliation are the two major types of herbivory forms on the plants. These two forms of predation by herbivores on plants cause different results. Some predators do not kill

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II

the plants or directly consume the tissues whereas some predators kill plants or destruct the parts of the plant by directly consuming the tissues.

The plant-herbivore interactions have substantial influence on the health of the habitat, the diversity and structure of the soil and plant communities. This type of predation may have positive impact on the communities or species such as herbivory up to a certain level increases the production and nutrient uptake by the plants as the feeding may remove aged leaves and roots triggering the growth of young shoots and roots that are more efficient in supporting the growth and developmental processes. The consumption of plants favours young foliage to fall down on ground contributing high quality of leaf litter with higher nutrient value to the soil. Trimming of the plants by the herbivores may cause seeds to fall down that are transported by the ants to their nests in the soil. The water and nutrient rich soil of ant’s nests offers favourable area for the successful seedling growth of plants. Moreover, plants pruned by the herbivores allow light to reach the ground and stimulate the growth of seeds by providing favourable surroundings. Furthermore, some plant-herbivore relationships offer protection to plants as shown by ant-acacia association. Herbivores adversely, sometimes advantageously, affect the plants; similarly plants have prominent effects on the fitness of their predators. Secondary metabolites are the plant substances that adversely affect the reproductive rate of herbivores. In the plant-herbivore association certain modes of defense are adopted by plants to counteract herbivore attacks which range from mimicry and chemical methods to structural features.

Herbivory is a two-edged sword, where both the interacting organisms have pronounced effects on each other’s fitness. Wide ranges of feeding opportunities are offered by the individual plant species and the dependent herbivore organisms developed many adaptations in form of specialized features and feeding strategies to consume their food source or plants. As an example, the adaptation of specialized features includes behavioural changes and modified mouthparts that allow herbivores to consume on plant species. To gain access to these tough and chemical plant tissues, external structures and water insoluble complex compounds several feeding strategies are employed by the herbivores including Alliance formation, Chewing mouthparts, Attack soft internal parts, Mining, Rostrum or tube-like mouthparts and Nectar feeding mouthparts etc. All animal posses a detoxifying mechanism against the chemical defense of secondary metabolites, called as mixed function oxidase (MFO). In order to utilize plants as their food source, the predators have to overcome the specialized features plants have adapted against their consumers. This type of interaction between plants and herbivores developed an arms race between them and lead to establishment of a strong relationship between them.

Principles of Ecology ZOOLOGY Prey predator and Plant herbivore interactions: Part II