Herbivores: Wikis

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A deer and two fawns feeding on some foliage

An herbivore is an animal that is adapted to eat plants.

Herbivory is a form of predation in which an organism consumes principally autotrophs[1] such as plants, algae and photosynthesizing bacteria. By that definition, many fungi, some bacteria, many animals, some protists and a small number of parasitic plants can be considered herbivores. However, herbivory is generally restricted to animals eating plants. Fungi, bacteria and protists that feed on living plants are usually termed plant pathogens (plant diseases). Microbes that feed on dead plants are saprotrophs. Flowering plants that obtain nutrition from other living plants are usually termed parasitic plants. More generally, organisms that feed on autotrophs in general are known as primary consumers.

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Herbivores

Leaf miners feed on leaf tissue between the epidermal layers, leaving visible trails

Herbivores form an important link in the food chain as they consume plants in order to receive the carbohydrates produced by a plant from photosynthesis. Carnivores in turn consume herbivores for the same reason, while omnivores can obtain their nutrients from either plants or herbivores. Due to an herbivore's ability to survive solely on tough and fibrous plant matter, they are termed the primary consumers in the food cycle(chain).

Evolution of herbivory

A fossil Viburnum lesquereuxii leaf with evidence of insect herbivory; Dakota Sandstone (Cretaceous) of Ellsworth County, Kansas. Scale bar is 10 mm.

Our understanding of herbivory in geological time comes from three sources: fossilized plants, which may preserve evidence of defence (such as spines), or herbivory-related damage; the observation of plant debris in fossilised animal faeces; and the construction of herbivore mouthparts.[2]

Long thought to be a Mesozoic phenomenon, evidence for herbivory is found almost as soon as fossils which could show it. Within under 20 million years of the first fossils of sporangia and stems towards the close of the Silurian, around 420 million years ago, there is evidence that they were being consumed.[3] Animals fed on the spores of early Devonian plants, and the Rhynie chert also provides evidence that organisms fed on plants using a "pierce and suck" technique.[2]

During the ensuing 75 million years[citation needed], plants evolved a range of more complex organs - from roots to seeds. There is no evidence for these being fed upon until the middle-late Mississippian, 326.4 million years ago. There was a gap of 50 to 100 million years between each organ evolving, and it being fed upon; this may be due to the low levels of O2 during this period, which may have suppressed evolution.[3] Further than their arthropod status, the identity of these early herbivores is uncertain.[3] Hole feeding and skeletonisation are recorded in the early Permian, with surface fluid feeding evolving by the end of that period.[2]

Arthropods have evolved herbivory in four phases, changing their approach to herbivory in response to changing plant communities.[4]
Another stage of herbivore evolution is characterized by the evolution of tetrapod herbivores, with the first appearance in the fossil record near the Permio-Carboniferous boundary approximately 300 MYA. The earliest evidence of herbivory by tetrapod organisms is seen in fossils of jawbones where dental occlusion (process by which teeth from the upper jaw come in contact with those in the lower jaw) is present. The evolution of dental occlusion lead to a drastic increase in food processing associated with herbivory and provides direct evidence about feeding strategies based on tooth wear patterns. Examination of phylogenetic frameworks reveals that dental occlusion developed independently in several lineages through dental and mandibular morphologes, suggesting that the evolution and radiation of tetrapod herbivores occurred simultaneously within various lineages.[5]

Predator-prey Theory (herbivore-plant interactions)

According to the theory of predator-prey interactions, the relationship between herbivores and plants is cyclic.[6] When prey (plants) are numerous their predators (herbivores) increase in numbers, reducing the prey population, which in turn causes predator number to decline.[7] The prey population eventually recovers, starting a new cycle. This suggests that the population of the herbivore fluctuates around the carrying capacity of the food source, in this case the plant.

Several factors play into these fluctuating populations and help stabilize predator-prey dynamics. For example, spatial heterogeneity is maintained, which means there will always be pockets of plants not found by herbivores. This stabilizing dynamic plays an especially important role for specialist herbivores that feed on one species of plant and prevents these specialists from wiping out their food source.[8] Prey defenses also help stabilize predator-prey dynamic, and for more information on these relationships see the section on Plant Defenses. Eating a second prey type helps herbivores’ populations stabilize[9]. Alternating between two or more plant types provides population stability for the herbivore, while the populations of the plants oscillate.[10] This plays an important role for generalist herbivores that eat variety of plants. Keystone herbivores keep vegetation populations in check and allow for a greater diversity of both herbivores and plants[9]. When an invasive herbivore or plant enters the system, the balance is thrown off and the diversity can collapse to a monotaxon system.[9]

Feeding strategies

Herbivores are limited in their feeding ability by either time or resources. Animals that are time limited, meaning they have a limited amount of time to consume the food they need, use a feeding strategy of grazing and browsing, while those animals that are resource limited, meaning that they are limited in the type of food they eat, use a selective feeding strategy. Grazers/browsers tend to be either very large herbivores that need to consume a lot of food in order to maintain their metabolism, or herbivores that have a very short amount of time to eat as much as possible before reproducing, like many generalist insects. Several theories attempt to explain and quantify the relationship between animals and their food, such as Kleiber's law, Holling's disk equation and Marginal Value Theorem.

Kleiber’s law explains the relationship between the size of the animal and the feeding strategy it uses. In essence, it says that larger animals need to eat less food, per unit weight, than smaller animals.[11] Kleiber’s law states that the metabolic rate (q0) of an animal is the mass of the animal (M) raise to the 3/4th power:
q0=M3/4
Therefore, the mass of the animal increases at a faster rate then the metabolic rate.[12]
There are many types of feeding strategies employed by herbivores. Many herbivores do not fall into one specific feeding strategy, but instead employ several strategies and eat a variety of plant parts.

Types of feeding strategies:

Feeding Strategy Diet Example
Frugivores Fruit Ring Tailed Lemur
Folivores Leaves Koalas
Nectarivores Nectar Honey Possum
Granivores Seeds Hawaiian Honeycreepers
Palynivores Pollen Bees
Mucivores Plant fluids, i.e. sap Aphids
Xylophages Wood Termites


Optimal Foraging Theory is a model for predicting animal behavior while looking for food or other resource, such as shelter or water. This model assesses both individual movement, such as animal behavior while looking for food, and distribution within a habitat, such as dynamics at the population and community level. For example, the model would be used to look at the browsing behavior of a deer while looking for food, as well as that deer’s specific location and movement within the forested habitat and its interaction with other deer while in that habitat.
This model can be controversial, where critics say that the theory is circular and untestable. Critics say that the theory uses examples that fit the theory, but that researchers do not use the theory when it does not fit the reality.[13] [14] Other critics point out that animals do not have the ability to assess and maximize their potential gains, therefore the optimal foraging theory is irrelevant and derived to explain trends that do not exist in nature.[15][16]

Holling’s disk equation models the efficiency at which predators consume prey. The model predicts that as the number of prey increases, the amount of time predators spend handling prey also increases and therefore the efficiency of the predator decreases.[17] In 1959 S. Holling proposed an equation to model the rate of return for an optimal diet: Rate (R ) = Energy gained in foraging (Ef)/(time searching (Ts) + time handling (Th))
R = Ef / (Ts + Th)
Where s = cost of search per unit time f = rate of encounter with items, h = handling time, e = energy gained per encounter
In effect, this would indicate that an herbivore in a dense forest would spend more time getting handling (eating) the vegetation because there was so much vegetation around than an herbivore in a sparse forest, who could easily browse through the forest vegetation. Therefore, according to the Holling's disk equation, the herbivore in the sparse forest would be more efficient at eating than the herbivore in the dense forest

Marginal Value Theorem describes the balance between eating all the food in a patch for immediate energy, or moving to a new patch and leaving the plants in the first patch to regenerate for future use. The theory predicts that absent complicating factors, an animal should leave a resource patch when the rate of payoff (amount of food) falls below the average rate of payoff for the entire area.[18] According to this theory, therefore, locus should move to a new patch of food when the patch they are currently feeding on requires more energy to obtain food than an average patch. Within this theory, two subsequent parameters emerge, the Giving Up Density (GUD) and the Giving Up Time (GUT). The Giving Up Density (GUD) quantifies the amount of food that remains in a patch when a forager moves to a new patch.[19] The Giving Up Time (GUT) is used when a animal continuously assesses the patch quality.[20]

Attacks and Counter-Attacks

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Plant Defense

A plant defense is a trait that increases plant fitness when faced with herbivory. This is measured relative to another plant that lacks the defensive trait. Plant defenses increase survival and/or reproduction (fitness) of plants under pressure of predation from herbivores.

Defense can be divided into two main categories, tolerance and resistance. Tolerance is the ability of a plant to withstand damage without a reduction in fitness. This can occur by diverting herbivory to non-essential plant parts or by rapid regrowth and recovery from herbivory. Resistance refers to the ability of a plant to reduce the amount of damage it receives from an herbivore. This can occur via avoidance in space or time[21], physical defenses, or chemical defenses. Defenses can either be constitutive, always present in the plant, or induced, produced or translocated by the plant following damage or stress[22].

Physical, or mechanical, defenses are barriers or structures designed to deter herbivores or reduce intake rates, lowering overall herbivory. Thorns such as those found on roses or acacia trees are one example, as are the spines on a cactus. Smaller hairs known as trichomes may cover leaves or stems and are especially effective against invertebrate herbivores[23]. In addition, some plants have waxes or resins that alter their texture, making them difficult to eat. Finally, some plants sequester silica inside their tissues. These are basically small pieces of glass that wear down the teeth of herbivores.

Chemical defenses are secondary metabolites produced by the plant that deter herbivory. There are a wide variety of these in nature and a single plant can have hundreds of different chemical defenses. Chemical defenses can be divided into two main groups, carbon-based defenses and nitrogen-based defenses.

Carbon-based defenses include terpenes and phenolics. Terpenes are derived from 5-carbon isoprene units and comprise essential oils, carotenoids, resins, and latex. They can have a number of functions that disrupt herbivores such as inhibiting adenosine triphosphate (ATP) formation, molting hormones, or the nervous system[24]. Phenolics combine an aromatic carbon ring with a hydroxyl group. There are a number of different phenolics such as lignins, which are found in cell walls and are very indigestible except for specialized microorgamisms; tannins, which have a bitter taste and bind to proteins making them indigestible; and furanocumerins, which produce free radicals disrupting DNA, protein, and lipids, and can cause skin irritation.

Nitrogen-based defenses are synthesized from amino acids and primarily come in the form of alkaloids and cyanogens. Alkaloids include commonly recognized substances such as caffeine, nicotine, and morphine. These compounds are often bitter and can inhibit DNA or RNA synthesis or block nervous system signal transmission. Cyanogens get their name from the cyanide stored within their tissues. This is released when the plant is damaged and inhibits cellular respiration and electron transport.

Plants have also changed features that enhance the probability of attracting natural enemies to herbivores. Some emit semiochemicals, odors that attract natural enemies, while others provide food and housing to maintain the natural enemies’ presence (eg. ants that reduce herbivory[25]). A given plant species often has many types of defensive mechanisms, mechanical or chemical, constitutive or induced, which additively serve to protect the plant, and allow it to escape from herbivores.

Herbivore Offense

Aphids are fluid feeders on plant sap.

The myriad of defenses displayed by plants means that their herbivores need a variety of techniques to overcome these defenses and obtain food. These allow herbivores to increase their feeding and use of a host plant. Herbivores have three primary strategies for dealing with plant defenses: choice, herbivore modification, and plant modification.

Feeding choice involves which plants an herbivore chooses to consume. It has been suggested that many herbivores feed on a variety of plants to balance their nutrient uptake and to avoid consuming too much of any one type of defensive chemical. This involves a tradeoff however, between foraging on many plant species to avoid toxins or specializing on one type of plant that can be detoxified.[26]

Herbivore modification is when various adaptations to body or digestive systems of the herbivore allow them to overcome plant defenses. This might include detoxifying secondary metabolites[27], sequestering toxins unaltered[28], or avoiding toxins, such as through the production of large amounts of saliva to reduce effectiveness of defenses. Herbivores may also utilize symbionts to evade plant defenses. For example, some aphids use bacteria in their gut to provide essential amino acids lacking in their sap diet[29].

Plant modification occurs when herbivores manipulate their plant prey to increase feeding. For example, some caterpillars roll leaves to reduce the effectiveness of plant defenses activated by sunlight[30].

The Adaptation Dance

The back and forth relationship of plant defense and herbivore offense can be seen as a sort of “adaptation dance” in which one partner makes a move and the other counters it[27]. This reciprocal change drives coevolution between many plants and herbivores, resulting in what has been referred to as a “coevolutionary arms race”[31]. The escape and radiation mechanisms for coevolution, presents the idea that adaptations in herbivores and their host plants, has been the driving force behind speciation[32][33].

It is important to remember that while much of the interaction of herbivory and plant defense is negative, with one individual reducing the fitness of the other, some is actually beneficial. This beneficial herbivory takes the form of mutualisms in which both partners benefit in some way from the interaction. Seed dispersal by herbivores and pollination are two forms of mutualistic herbivory in which the herbivore receives a food resource and the plant is aided in reproduction[34].

Impacts of Herbivores

The impact of herbivory can be seen in many areas ranging from economics to ecological, and sometimes affecting both. For example, environmental degradation from white-tailed deer (Odocoilus virginianus) in the U.S. alone has the potential to both change vegetative communities through over-browsing and cost forest restoration projects upwards of $750 million annually. Agricultural crop damage by the same species totals approximately $100 million every year. Insect crop damages also contribute largely to annual crop losses in the U.S.[35] Another area in which herbivory greatly affects economics is through the revenue generated by recreational uses of herbivorous organisms, such as hunting and ecotourism. For example, the hunting of herbivorous game species such as white-tailed deer, cottontail rabbits, antelope, and elk in the U.S. contributes greatly to the billion-dollar annually hunting industry. Ecotourism is another major source of revenue, particularly in Africa, where many large mammalian herbivores such as elephants, zebras, and giraffes help to bring in the equivalent of millions of US dollars to various nations annually.

See also

References

  1. ^ Campbell, N. A. (1996) Biology (4th edition) Benjamin Cummings, New York ISBN 0-8053-1957-3
  2. ^ a b c Labandeira, C.C. (1998). "Early History Of Arthropod And Vascular Plant Associations 1". Annual Reviews in Earth and Planetary Sciences 26 (1): 329–377. doi:10.1146/annurev.earth.26.1.329. 
  3. ^ a b c Labandeira, C. (2007). "The origin of herbivory on land: Initial patterns of plant tissue consumption by arthropods". Insect Science 14 (4): 259–275. doi:10.1111/j.1744-7917.2007.00152.x. 
  4. ^ Labandeira, C.C. (2005). "The four phases of plant-arthropod associations in deep time" (Free full text). Geologica Acta 4 (4): 409–438. http://www.geologica-acta.com:8080/geoacta/pdf/vol0404a01.pdf. Retrieved 2008-05-15. 
  5. ^ Origin of dental occlusion in tetrapods: signal for terrestrial vertebrate evolution? Journal of Experimental Zoology Part B: Molecular and Developmental Evolution. Volume 306B Issue 3, Pages 261 - 277 Special Issue: Vertebrate Dentitions: Genes, Development and Evolution Published Online: 8 May 2006 Copyright © 2008 Wiley-Liss, Inc., A Wiley Company Robert R. Reisz * Department of Biology, University of Toronto at Mississauga, Mississauga, Ont., Canada L5L 1C6
  6. ^ Gotelli, NJ. A Primer of Ecology. Sinauer Associates Inc., Mass. 1995
  7. ^ Gotelli 1995
  8. ^ Smith, RL and Smith, TM. Ecology and Field Biology: Sixth Edition.Benjamin Cummings, New York. 2001
  9. ^ a b c Smith and Smith, 2001
  10. ^ Gotelli, 1995
  11. ^ Nugent G, Challies CN. 1988. Diet and food preferences of white-tailed deer in north-eastern Stewart Island. New Zealand Journal of Ecology 11: 61-73.
  12. ^ Nugent and Challies, 1988
  13. ^ Pierce, G. J. and J. G. Ollason. 1987. Eight reasons why optimal foraging theory is a complete waste of time. Oikos 49:111-118.
  14. ^ Stearns, S. C. and P. Schmid-Hempel. 1987. Evolutionary insights should not be wasted. Oikos 49:118-125
  15. ^ Lewis, A. C. 1986. Memory constraints and flower choice in Pieris rapae. Science 232:863-865
  16. ^ Janetos, A. C. and B. J. Cole. 1981. Imperfectly optimal animals. Behav. Ecol. Sociobiol. 9:203-209
  17. ^ Stephens, D. W. and J. R. Krebs. 1986. Foraging theory. Princeton University Press
  18. ^ Charnov, E. L. 1976. Optimal foraging, the marginal value theorem. Theor. Pop. Biol.-9:129-136.
  19. ^ Brown, J. S., B P. Kotler and W A. Mitchell. 1997. Competition between birds and mammals: a comparison of giving-up densities between crested larks and gerbils. Evol. Ecol. 11:757-771.
  20. ^ Breed, M. D. R. M. Bowden, M. F. Garry, and A. L. Weicker. 1996. Giving-up time variation in response to differences in nectar volume and concentration in the giant tropical ant, Paraponera clavata. J. Ins. behav. 9:659-672
  21. ^ Milchunas, D.G. and I. Noy-Meir. 2002. Grazing refuges, external avoidance of herbivory and plant diversity. Oikos 99(1): 113-130.
  22. ^ Edwards P.J. and S.D. Wratten. 1985. Induced plant defences against insect grazing: fact or artefact? Oikos 44(1):70-74.
  23. ^ Pillemer, E.A. and W.M. Tingey. 1976. Hooked Trichomes: A Physical Plant Barrier to a Major Agricultural Pest. Science 193(4252): 482-484.
  24. ^ Langenheim, J.H. 1994. Higher plant terpenoids: a phytocentric overview of their ecological roles. Journal of Chemical Ecology 20: 1223-1280.
  25. ^ Heil, M., T. Koch, A. Hilpert, B. Fiala, W. Boland, and K. Eduard Linsenmair. 2001. Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proceedings of the National Academy of Sciences 98(3): 1083-1088.
  26. ^ Dearing, M.D., A.M. Mangione, and W.H. Karasov. 2000. Diet breadth of mammalian herbivores: nutrient versus detoxification constraints. Oecologia 123: 397-405.
  27. ^ a b Karban, R. and A.A. Agrawal. 2002. Herbivore Offense. Annual Review of Ecology and Systematics 33:641-664.
  28. ^ Nishida, R. 2002. Sequestration of Defensive Substances from Plants by Lepidoptera. Annual Review of Entomology 47:57-92.
  29. ^ Douglas, A.E. 1998. Nutritional Interactions in Insect-Microbial Symbioses: Aphids and Their Symbiotic Bacteria Buchnera. Annual Review of Entomology 43:17-37.
  30. ^ Sagers, C.L. 1992. Manipulation of host plant quality: herbivores keep leaves in the dark. Functional Ecology 6(6):741-743.
  31. ^ Mead, R.J., A.J. Oliver, D.R. King and P.H. Hubach. (1985). The Co-Evolutionary Role of Fluoroacetate in Plant-Animal Interactions in Australia. Oikos 44(1): 55-60.
  32. ^ Ehrlich, P. R. and P. H. Raven. 1964. Butterflies and plants: a study of coevolution. Evolution 18:586-608.
  33. ^ Thompson, J. 1999. What we know and do not know about coevolution: insect herbivores and plants as a test case. Pages 7–30 in H. Olff, V. K. Brown, R. H. Drent, and British Ecological Society Symposium 1997 (Corporate Author), editors. Herbivores: between plants and predators. Blackwell Science, London, UK.
  34. ^ Herrera, C.M. 1985. Determinants of Plant-Animal Coevolution: The Case of Mutualistic Dispersal of Seeds by Vertebrates. Oikos 44(1): 132-141.
  35. ^ AN INTEGRATED APPROACH TO DEER DAMAGE CONTROL Publication No. 809 West Virginia Division of Natural Resources Cooperative Extension Service Wildlife Resources Section West Virginia University Law Enforcement Section Center for Extension and Continuing Education March 1999

Further reading

  • Bob Strauss, 2008, Herbivorous Dinosaurs, The New York Times
  • Danell, K., R. Bergström, P. Duncan, J. Pastor (Editors)(2006) Large herbivore ecology, ecosystem dynamics and conservation Cambridge, UK : Cambridge University Press. 506 p. ISBN 0521830052
  • Crawley, M. J. (1983) Herbivory : the dynamics of animal-plant interactions Oxford : Blackwell Scientific. 437 p. ISBN 0632008083
  • Olff, H., V.K. Brown, R.H. Drent (editors) (1999) Herbivores : between plants and predators Oxford ; Malden, Ma. : Blackwell Science. 639 p. ISBN 0632051558

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