Character Displacement

1. Character Displacement Character displacement occurs when interspecific competition leads to the selection of different characteristics (usually morphological) in the zone of geographical overlap of species. What shifts is the morphology of some aspect of the species important in interactions. The classic example is in Darwin’s Galapagos finches:

2. Geospiza fortis Geospiza fulginosa

3. Since food resources are commonly the limiting resource over which competition occurs, the morphology of feeding structures is the feature frequently 'displaced'. Grant (1968) drew comparisons of wing size and bill size among closely related species on islands and made parallel comparisons between some of the same species when both were present in mainland habitats. The differences found clearly indicate both greater difference between species in their bill sizes than their wing lengths (competition is for food), and that differences are greater on islands than on nearby mainland. Here is some of Grant’s data extracted from summary tables:

4. % differences in characteristics between congeneric species Species Mainland Island wing bill wing bill Parus 4.0 28.2 2.7 55.9 atricapillus/hudsonicus Hylocichla 5.8 9.2 8.4 13.0 guttata/ustulata Centurus 24.2 47.7 33.5 63.9 aurifrons/pygmaeus Platypsaris 9.4 8.3 11.8 17.7 aglaiae/bidentata Cynanthus 11.6 9.5 32.6 28.1 latirostris/A.rutila These species are all present on Pacific islands near and on mainland of California and Mexico.

5. What happens if the survey is across a wider range of geographic areas? Answer: the same basic pattern… Island Species % Difference in: wing bill Norfolk Zosterops 8.6 16.7 lateralis/albogularis Lord Howe Zosterops 9.8 36.4 strenua/lateralis Tristan de Nesospiza 16.3 33.3 Cunha wilkinsi /acunhae Ongea levu Mayrornis 10.1 19.1 lessoni/versicolor Kauai Laxops 13.4 50.0 parva/virens Socotra Onchyognathus 7.2 20.2 frater/blythii

6. Island Species % Difference in: wing bill Celebes Dicrurus 16.4 22.6 (Sulawesi) montanus/hottentottus Andaman Dicrurus 19.8 19.0 paradiseus/andamanensis Tasmania Acanthiza 0.0 16.2 pusilla/ewingi Mauritius Zosterops 6.8 17.1 mauritiana/curvirostris These differences, plus many others that could be cited, demonstrate that food is frequently a limiting resource, and that the world is not so green as Hairston et.al. claimed.

7. Kauai Sulawesi Norfolk Mauritius Tristan de Cunha Lord Howe Tasmania

8. Food as a Limiting Resource Recognizing that limits to the food resource can limit population size is straightforward. The question remains - Can food regulate populations? The problem with most field studies of 'regulation' of populations by their food resources is lack of a proper control. To establish regulation in the proper sense, population density must tend toward an equilibrium from both above and below as food resources change. There is one field study which attempts to demonstrate that - a study in which both the density of Lymnaea elodes and food resources were manipulated.

9. In the field, all measurements must be taken relative to an unmanipulated control treatment. Eisenberg did that, fencing off areas at the margin of a pond in southeastern Michigan, and maintaining three kinds of areas: • control, • areas in which snail density was reduced to 1/5 of control, • and • 3) areas where density was increased to 5x control. • 4) In additional replicate pens 10 oz. packages of frozen spinach every 4 days.

10. The life history of the snails: Lymnaea produces only 1 generation per year, laying eggs in gelatinous egg masses on the surfaces of vegetation. The eggs hatch during the summer and grow to 1-5 mm shell diameter. Overwintering (estivation) occurs as small juveniles by burrowing into the mud along pond margins. In the spring they emerge and grow to reproductive adulthood as the pond thaws and spring runoff submerges the margins where estivation occurred. Reproduction occurs through June an July. That means there are only two basic size classes in the pond at any time, young of the year and adults from the previous year, which are easily separated.

11. Density manipulations revealed rapid regulation. It is evident in egg laying by adults in the summer following density treatment. It's evident both in the total numbers of eggs in pens, and in the number of eggs per egg mass. The total number of eggs produced per pen shows no relationship to adult density, but the number of egg masses, and particularly the number of eggs per egg mass show essentially perfect density compensation. Adult and juvenile survivorship thus show little or no response, but mx or fecundity showed a strong response. This response does not implicate food.

12. The key to demonstrating that food was the regulating factor is the effect of adding only 10 oz of spinach every 4 days to a 1x5 m pen. In those pens there was a 25x increase in the number of eggs laid, with increases evident in both the number and size of egg masses. Pens are 'filled' with aquatic vegetation, therefore it wasn't food quantity, but quality which was the limiting factor. Does adult density the following year increase 25x? No, lx in 'fed' pens also changed, so that the number of juveniles estivating was increased only by 2x. Hairston et al.'s hypothesis that 'the world is green' is not warranted from the herbivores' point of view. There are other reasons why plant quality may suggest food limitation. They include the various forms plant defenses can take.

13. Chemical Defenses There are 3 broad classes into which we can pigeonhole chemical defenses: 1) toxic substances, 2) substances which reduce the digestibility or effective quality of consumed food, and 3) pharmaco-active substances. Most chemical defenses (other than tannin production) are offshoots of normal metabolic pathways in the leaves. An outline of 'normal' and secondary product metabolism reveals that there is a close metabolic relationship among many toxic, pharmacoactive and inhibitory defenses.

14. Sugar metabolism Amino acid metabolism acetate phenolics  tannins quinones quinones waxes alkaloids terpenes glycosides steroids glucosinolates Many plant chemical defenses against insect herbivores have their origins as simple oxidations (or other modifications) of ordinary phenolics, for example: the active ingredient in cinnamon - trans cinnamic acid the active ingredient in aspirin - salicyclic acid the active ingredient in coffee - caffeic acid and a related flavenoid: the active ingredient in vanilla - vanillic acid and a quinone produced from simple phenols: don't plant things under a walnut tree - juglone

15. Vanilla planifolia And raw vanilla beans Cinnamomum zeylandicum and its bark Salix babylonicum and aspirin

16. Toxic Defenses Are there characteristic kinds of plants or plant tissues in which different kinds of plant chemical defenses predominate? Cates (1977, 1980) suggests there are general patterns: Toxins are more frequently characteristic of ephemeral tissues of plants (e.g. flowers, young leaves) which the plant cannot afford to lose. These tissues are, however, less predictable in time and space since they are ephemeral. As a result, herbivores successful in utilizing plants or tissues protected by toxins are likely to be specialists who have evolved the ability to detoxify the protection, and related plants are likely to have individualized (by species) defenses.

17. Toxins directly affect metabolic processes in the herbivores, are easily absorbed by animal target systems, and are active in low concentrations. They represent generally < 2% of plant tissue dry weight. If the plant, or the endangered tissue, is unpredictable in time and/or space, then damage from the specialist herbivore is limited due to difficulty in finding this plant or tissue. Ephemerality selects for generalist herbivores, in that they are not searching, but feeding on encounter. Since detoxification (and the evolution of the capability) is expensive and 'difficult', toxic defenses will be most effective against generalists, particularly if the defenses deviate widely from the already extant or ‘average' pattern present in the community.

18. From the point of view of the herbivore - the generalist herbivore feeds from a wide variety of plants as a strategy. In doing that, while avoiding eating intensively from any single food source, the limited detoxification capabilities which these herbivores have is not overwhelmed by any single defensive chemical. For the apparent/persistent plant tissue the direct defense needed is one against a specialist herbivore, which, having encountered the tissue, would feed heavily on it. Each species of plant evolves independently, but convergence has been shown to occur. Within plant taxa many species have patterns of digestibility-reducing defenses in common. The costs and amounts of defensive chemical may be high.

19. There is an evolutionary race between toxin evolution and the evolution of detoxification capability. Liver microsomal enzymes are responsible for much of the detoxification. Occasionally the process turns on the herbivore: If caterpillars were classified by the number of plant families on which they fed into monophagous (1 plant family), moderately polyphagous (2-10 families) and highly polyphagous (11 or more families), the activities of microsomal oxidase activites paralleled diet breadth. Activities were measured by the conversion of dieldrin to aldrin, and were 20.4, 90.7 and 294.4 nanograms processed per milligram of enzyme per minute respectively.

20. The oxidation of certain toxins, dieldrin among them, produces a 'de-toxified‘ molecule which, in many animals, is more toxic than the environmental chemical. In other cases, e.g.Brassica (cabbages), a diversity of herbivores and their predators are attracted to the plants by the mustard oil present in leaves as an anti-herbivore chemical toxin. An example of diversity in toxic defenses in related species is alkaloids in Lupinus species of the southwestern U.S. Species Alkaloids A B C D E F G H Lupinus arboreus 3 1 2 1 L. chamissonis 2 1 1 L. arbifrons 1 1 1 L. excubitus 1 1 1 1 1 1 1 L. niveus 1 L. latifolius 2

21. Digestibility Reducing Defenses Digestibility reducing substances are generally protein or carbohydrate complexing agents that prevent or reduce digestion of food materials from plant tissues. They are characteristic of mature tissues of perennials, particularly woody plants. In those tissues a surprisingly large fraction of biomass can be defensive chemicals. 80% of woody dicot perennials contain tannins, while only 15% of annuals and non-woody dicot perennials contain tannins. Digestibility reducers are generalized compounds, both in terms of the breadth of the targeted herbivore spectrum and in terms of the variety of plant species using similar or identical chemicals.

22. Compare alkaloid distribution to the distributions of different tannins in the leaves of maple (Acer) species… Species Tannins A B C D E F G H Acer ginnale A. tartaricum + + + + + A. saccharinum A. platanoides A. campestre + + A. rubrum A. pennsylvanicum A. spicatum A. rotundilobum + A. griseum A. saccharum A. pseudoplatanus

23. Common names of (some) of those maple species: • tartaricum – tartar maple • A. saccharinum – silver maple • platanoides – Norway maple • A. campestre – field maple • rubrum – red maple • A. pennsylvanicum – striped maple • A. spicatum – mountain maple • A. griseum – paperbark maple • saccharum – sugar maple • A. pseudoplatanus – sycamore maple

24. Thus far chemical defenses have been considered as constitutive, that is defenses prepared and maintained whether the herbivore is present or not. There is also evidence of inducible defenses, i.e. those synthesized only in response to 'initial' herbivore damage. The existence of an inducible defense has been intensively studied in arctic birch (personal interest here!), which is a favorite forage of caribou (reindeer) in northern Europe. We’re not interested in reindeer. The herbivore that can defoliate entire trees of some strains of northern birch is the autumnal moth Oporina (now called Epirrita) in outbreaks.

25. Eppirita autumnata – the defoliating moth Betula pendula – the birch common in northern Scandanavia

27. How do birch trees respond to herbivory? There are a number of responses, including induction of defensive chemicals. Responses include: a) By escape in time. The tree is perennial; it certainly suffers from herbivory, but even defoliation in a single year does not result in certain mortality. Instead, there are a number of responses evident in the following year. There is delay and increased variability in the date of leafing out the following spring. Measured as standard deviations in the date of leaf burst, in control plants (not defoliated) the s.d. was .32 days, but in defoliated plants it was .88 days. Larval hatching from overwintering eggs had s.d.'s of .73 or less, decreasing as temperature increased. The difference in variability makes larval starvation more likely in years following defoliation.

28. b) By inducible chemical defense. Mechanical damage to leaves, for example by larval chewing, increases the amount of phenol (the particular chemical is called platyphylloside) in the leaves. Induction occurs in less than 48 hours. Damaged leaves, gathered 48 hours after damage occurred, had 9% more phenol than undamaged leaves on the same plant. Those phenols have important effects. Measurement of inhibition of trypsin, a key enzyme in protein digestion, indicate undamaged leaf extract reduces trypsin activity by 23% (even undamaged leaves carry some chemical defenses), but induced leaves reduce activity by 32%, or an increase in trypsin inhibition by 40%. Thus, the ability to digest protein has been significantly reduced.

29. This inhibition slows the growth of larvae both following initial induction and in the following year. The platyphylloside is effective in inhibiting digestion down to a concentration of 0.8% in leaf tissue. That is a concentration lower than is observed in even undamaged leaves. c) These defensive adaptations don't disappear rapidly after coming into play. The relaxation time for these defenses may be as long as 3-4 years. Larvae reared in 1979 on trees artificially defoliated in 1975-6 were still significantly lighter (smaller due to slower growth, presumably due to inhibitory defenses) than those grown on leaves from control plants.

30. This picture may not be as general as European studies of arctic birches might suggest… • Chapin et al.(1985) searched for parallel responses in the woody plants of Alaska and found none. Simulated herbivory did not induce increased production of phenols, resins, or tannins in Alaskan plants including willows, poplars, aspens, or birch. • Even the basic pattern of digestibility-reduction by tannins has been found to have exceptions. • Some arctic ruminants have salivary proteins that bind • (complex) tannins as leaves are initially chewed, so that the defensive function of the tannins is circumvented.

31. b) Bernays (1980) found growth and survivorship of locusts differs among species exposed over evolutionary time to diets including different frequencies and abundance of tannins. She studied 15 locust species ranging from monophagous to highly polyphagous species. Most of the locust species feed on grasses in nature, and were maintained in the laboratory and tested using a grass, wheat. For tests of tannic acid effects the wheat leaves were dipped in tannic acid solution. Other species feed on dicots in nature; they were maintained and tested using lettuce leaves instead of wheat. Four groups of locust species were distinguished in terms of their responses to tannic acid:

32. Group 1) Tannic acid caused complete mortality during early instars. In these locusts protein complexing by tannins is unimportant to its effect. Instead, tannic acid had dramatic histological consequences; lesions were rapidly apparent in the insects' midgut. Tannic acid then entered the open circulatory system and acted as a systemic poison. As a group these locusts are characteristically grass feeders; grasses rarely contain tannins naturally, and the locusts are unlikely to have been exposed to tannins in their natural diets

33. Group 2) Mortality is delayed to later instars, and a few individuals molt successfully to adulthood. These species are also generally grass-feeders and inexperienced with tannins. Their weights as late instar larvae are severely reduced, probably reflecting protein complexing by dietary tannins. One example is Acrida conica. 50 first instar larvae constituted each group. Survival and weight (mg) of survivors were: Treated Control Male Female Male Female weight 146 + 4 396 216 + 6 623 + 10 number surviving 10 2 1 19 There must be a miscopied number here. There is no SD with only 1 survivor.

34. Group 3) These species showed no significant effect on survival. They are generally polyphagous, and therefore had been exposed to at least a moderate proportion of dicots containing tannins in their natural diets. Digestibility, digestive efficiency and weight increase also seemed unaffected by tannins. A good example of this category is the plague locust, Schistocerca gregaria: Treated Control Male Female Male Female weight (mg) 1093 + 24 1343 + 20 1110 + 16 1319 + 15 number surviving 31 28 29 28 digestibility (%) 34 + 4 34 + 3 digestive efficiency 38 + 6 34 + 7 % wt.inc. (last instar) 79 + 5 69 + 8

35. Group 4) A few species (two in these studies) do better on tannins than without. Both species are specialist feeders; their normal diets consist of the leaves of tropical acacias, which are loaded with just the sort of tannin used in these experiments. At least for these two species there is the suggestion of enzymatic hydrolysis of tannins (and possibly other related phenolics) into compounds useful in normal metabolic pathways. Example: Anacridia melandorhodum Treated Control Male Female Male Female weight 1517 + 30 2124 + 37 1314 + 42 1813 + 67 survival 22 20 8 11 digestibility 52 + 2 40 + 4 efficiency 25 + 2 20 + 2% wt. inc. last instar 116 + 6 103 + 5