BIOS 3010: Ecology. Laboratory 7. Dr Stephen Malcolm, Dept. Biological Sciences, WMU
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1 BIOS 3010: Ecology Laboratory 7 Dr Stephen Malcolm, Dept. Biological Sciences, WMU Goldenrod galls: An analysis of herbivory and natural enemy attack through 3 trophic levels. Goldenrod (Solidago altissima/ S. canadensis) Bios 3010: Ecology labs 7 and 8 Page - 1
2 FIELD OBSERVATIONS Introduction Goldenrod is a familiar and abundant feature of the autumn landscape in southwestern Michigan. As such it supports an intriguing and predictable community of interacting organisms and provides a wealth of opportunities to examine various concepts in ecology. In particular, the goldenrod gall fly Eurosta solidaginis commonly attacks Canadian or tall goldenrod as a gall-making herbivore and supports a complex of natural enemies that include insect parasitoids and bird predators. Because the 'ball galls' of E. solidaginis are obvious and common, the system offers useful opportunities to measure various ecological concepts, including: (1) density dependence (2) spatial distribution of herbivore and natural enemy attack (3) impact of herbivory on host plant reproduction (4) impact of natural enemy attack on host plant reproduction, mediated via the herbivore Background As long ago as 1947, George Varley published an influential paper on the population trends and mortality factors of the knapweed gall-fly in England. His work coincided with Deevey's life table research and together they showed the importance of mortality and fecundity schedules for descriptions of animal population growth and fluctuation. The knapweed gall-fly system is remarkably similar to the goldenrod ball gall system and offers us the opportunity to gather some insight into how a system operates - especially one that bridges the three trophic levels of plant, herbivore and natural enemies. The plant-herbivore interaction: The common round galls, or 'ball galls' on Canadian goldenrod, Solidago canadensis (or tall goldenrod, S. altissima = S. canadensis var scabra), are caused by one species of tephritid fly, Eurosta solidaginis. The short-lived adult fly emerges from the gall in late May to early June, mates and then lays eggs on the terminal buds of goldenrod (Abrahamson et al., 1983; Abrahamson & Weis, 1997). After 7-12 days the larva emerges and bores into the meristematic tissue and initiates the formation of a ball gall. By mid September the larva is full grown (note: timing may vary according to the accumulation of day-degrees = Bios 3010: Ecology labs 7 and 8 Page - 2
3 physiological time integrating temperature and time) and it overwinters as a diapausing larva. The larva pupates inside the gall the following April. Please view the attached PowerPoint presentation about the system. Natural enemies of the goldenrod gall fly: Two hymenopteran parasitoids in the family Eurytomidae can cause 40-60% mortality of Eurosta solidaginis larvae (Abrahamson, 1977; Abrahamson et al., 1983; Abrahamson & Weis, 1997). Eurytoma obtusiventris causes Eurosta to pupate in mid August instead of April and its larva eats the fly and remains inside the puparium until spring. Another eurytomid wasp, Eurytoma gigantea, eats the fly larva and also eats some of the gall before pupating and emerging in the spring. In addition a predatory beetle larva, Mordellistena unicolor (Mordellidae) bores in the wall of the gall and occasionally eats the fly larva. As well as these insect parasitoids, bird predators peck open the galls to feed on the larvae of Eurosta. Both black-capped chickadees, Parus atricapillus, and downy woodpeckers, Picoides pubescens, peck open large galls (Abrahamson et al., 1989). The exercise: Please view more figures here. The presence of ball galls on goldenrod may vary with plant distribution and abundance so that plant age (distribution in time), distance between plants (distribution in space) and plant density (abundance) will influence the occurrence of ball galls. In turn, these spatial and temporal differences will influence attack by natural enemies because of variation in their costs of foraging and attacking the gall-making herbivore. Gall diameters may vary with plant age and size and possibly with plant density (because of intraspecific competition for resources). Larger, thick walled galls may also provide better protection for the gall fly from wasp parasitoids than smaller, thin-walled galls - the wasp parasitoids are tiny and have ovipositors of limited length to penetrate the gall wall and lay an egg in or on the fly larva. We know from Abrahamson et al. (1989) that the wasp parasitoid Eurytoma obtusiventris and the beetle predator, Mordellistena unicolor, can attack galls of all diameters, but that the wasp, Eurytoma gigantea, prefer to attack small galls and the bird predators prefer to attack large galls. In addition, the birds are vulnerable to attack by their natural enemies, such as Cooper's and sharp-shinned hawks and so the distance of galls from cover, or the height of a gall from the ground might also influence whether or not chickadees and woodpeckers will peck open the galls for the fly larvae. Bios 3010: Ecology labs 7 and 8 Page - 3
4 In summary, therefore, you should aim to tell a story centered on the goldenrod gall fly and its ball gall that shows how features of the plant population influence attack of the fly inside its gall by natural enemies at the third trophic level. Methods The class should divide into 5 groups of approximately 4 people in each group. Each group should identify two 10m x 10m quadrat areas of goldenrod - one with an edge within 10m of shrub or tree cover and the other with an edge no less than 30m from shrub or tree cover. A) Make the following measurements with a tape and add the data to the linked datasheet: (1) Distance of the quadrat edge nearest to cover should be measured for each 100m 2 quadrat area. (2) In each 100m 2 quadrat the goldenrod stems should either be counted as an absolute estimate of stems.100m -2, or subsampled with randomly selected, smaller quadrats if the density is extremely high. (3) In each 100m 2 area, 20 measurements should be taken of the nearest neighbor distance measured at ground level between the two stem bases that are closest. (4) For these same 20 plants also measure their height from ground level to the highest point of each plant and their diameter at ground level. Make sure that these measurements are of ungalled plants. B) Locate all plants with ball galls: Identify all plants with ball galls of the goldenrod gall fly, Eurosta solidaginis (see figure 1b) and check the identity of the plants as either Solidago canadensis canadensis, with sparse pubescence, 2-3 mm flowers and sharply serrate leaves, or Solidago canadensis scabra (=Solidago altissima) with relatively dense pubescence, flowers larger than mm and sparsely toothed leaves (Note: "ball galls" are large, obviously round galls that should not be confused with "elliptical galls" or "rosette galls." Elliptical galls are caused by larvae of the moth, Gnorismoschema gallaesolidaginus, and are usually found lower down the stem of goldenrod than the ball gall. This means that elliptical galls are initiated earlier than ball galls. Bios 3010: Ecology labs 7 and 8 Page - 4
5 Rosette galls are caused by the midge, Rhopalomyia solidaginis, which causes a proliferation of leaves at the tip of the growing stem forming a dense rosette. Code number each galled plant according to its 100m 2 quadrat and record the following: (1) The number of ball galls, elliptical galls and rosette galls in each 100m 2 quadrat. (2) The nearest neighbor distance of each galled plant to (a) its nearest galled neighbor and (b) to its nearest ungalled neighbor. (3) The height of each galled plant from ground level to the highest point and its diameter at ground level. (4) The height of the center point of each gall from ground level (5) For all galled plants, and the sample of 20 plants in A(4) above, measure (a) their basal stem diameter in mm with calipers. Use this measurement plus stem height (A4 above) to calculate (b) an index of plant biomass as, basal area (basal stem diameter x p) x stem height. (Note: make sure that measurements are attributed to code numbered plants). C) Collection of plant material for further analysis. (1) Carefully cut the 20 ungalled plant stems from each 100m 2 quadrat in A(4) and B(5) at ground level. (2) Carefully cut all galled plant stems (include any elliptical and rosette galls with the ball galls) from each 100m 2 quadrat in A(4) and B(5) at ground level. OBSERVATIONS Methods: Using the material you have collected, cut each gall from the plant stems and make sure that you know its coded identity. Then carefully dissect each ball gall and record the presence of the following (use the two sets of linked illustrations 1 and 2): (1) Intact larvae of Eurosta solidaginis, the goldenrod gall fly (see figure 2) (2) Large puparium of the goldenrod gall fly that should contain the larva or puparium of the wasp parasitoid Eurytoma obtusiventris (the internal parasite that causes premature pupation at about mid August in Eurosta), see figure 1. The parasite's puparium is Bios 3010: Ecology labs 7 and 8 Page - 5
6 about 7.4 x 2.2 mm and is several times smaller than the host larva or the true puparium of the host. (3) White fleshy larva of the external parasite Eurytoma gigantea (see figure 3). This parasite consumes that gall fly larva by the end of August and remains in the cavity until spring when it pupates. The gall fly cavity is usually enlarged by Eurytoma gigantea and is filled with large, black pellets of excreted frass. (4) Slender white larvae of the beetle, Mordellistena unicolor (see figure 4) this may occur in the gall as either an inquiline (a codweller in the gall) or more usually as a predator of Eurosta (record whether Eurosta has been eaten if you find this beetle). (5) Evidence of bird predation - a conical hole to the center of the gall caused by black-capped chickadees or downy woodpeckers. Check to see whether Eurosta or any other larva is present or absent - i.e. whether predation was successful or whether it was aborted prior to reaching the gall insect's chamber. Chickadees may make a larger, more ragged hole than the neat, conical hole made by downy woodpeckers (see figure 5). (6) Unknown mortality or unformed gall etc. Communication of your results Tabulate all your results from both field and laboratory observations and hand your results during the lab to your TA. We will tabulate the class results for all <15 independent replicates of the experiment (results from 5 groups of <4 people for 3 labs) and return these collated results to you. You should then use these class results and the references listed below to write a 4 page paper discussing the ecological implications of the results from the two labs. In other words, communicate the story - science is not worth doing until it has been communicated (even Darwin had to be cajoled and bullied to publish)! References (with library locations) Abrahamson, W.G Solidago canadensis galls: A study of interacting natural populations. Pages in L.B. Crowder (editor), Ecological Lab Experiences: An Ideas Forum. Department of Zoology, Michigan State University, East Lansing, Michigan. (not available - all the information is in this handout) Abrahamson, W.G., Armbruster, P.O., & Maddox, G.D Numerical relationships of the Solidago altissima stem gall insect-parasitoid guild food chain. Oecologia 58: (QH540.O33x) Abrahamson, W.G., Sattler, J.F., McCrea, K.D., & Weis, A.E Variation in selection pressures on the goldenrod gall fly and the competitive Bios 3010: Ecology labs 7 and 8 Page - 6
7 interactions of its natural enemies. Oecologia 79: (QH540.O33x) Abrahamson, W.G., & Weis, A.E Evolutionary ecology across three trophic levels. Goldenrods, gallmakers, and natural enemies. Princeton University Press, Princeton, NJ. 456 pages (QL 537.T42 A ) Varley, G.C The natural control of population balance in the knapweed gall-fly (Urophora jacaena). The Journal of Animal Ecology 16: (QL750.J65 - worth looking at as a classic and its relevance to our considerations of population dynamics, rather than for its immediate relevance to this exercise) Weis, A.E., & Abrahamson, W.G Potential selective pressures by parasitoids on a plant-herbivore interaction. Ecology 66(4): (QH540.E3) Weis, A.E., & Abrahamson, W.G Evolution of host-plant manipulation by gall makers: Ecological and genetic factors in the Solidago-Eurosta system. The American Naturalist 127: (QH1.A5) Bios 3010: Ecology labs 7 and 8 Page - 7
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