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Oecologia

Oecologia

Oecologia.

Coevolution: Patterns of legume predation by a Iycaenid butterfly

10 2

1972

99- 0029-8549

[TN :322108][ODYSSEY: 140.233.2.27/MDY]

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This material may be protected by copyright law (Title 17 U.S. Code) System Date/Time: 2/21/20111:59:32 PM MST

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International Association for Ecology

Coevolution: Patterns of Legume Predation by a Lycaenid Butterfly Author-Is): D. E. Breedlove and P. R. Ehrlich

Source: Oecologie, Vol. 10, No.2 (1972), pp. 99-104

Published by: Springer in cooperation with International Association for Ecology Stable URL: http://www.jstor.org/stable/4214781

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Oecologia (Berl.) 10, 99-104 (1972) © by Springer- Verlag 1972

Coevolution: Patterns of Legume Predation by a Lycaenid Butterfly

D. E. Breedlove and P. R. Ehrlich

Received October 4, 1971

Summary. Perennial legumes in Gunnison County, Colorado suffer heavy differential flower predation by larvae of a lycaenid butterfly. The butterfly populations may be resource-limited, and seem in tum to be an important factor in the evolution and distribution of the various legume species.

There is a growing body of evidence on the importance of herbivore predation in plant evolution and in determining plant abundance (Ehrlich and Raven, 1965; Janzen, 1966, 1969; Ehrlich, 1970; Janzen, 1970, 1971), including the demonstration that the flower-feeding lycaenid butterfly Glaucopsyche lygdamus Doubleday may have a substantial impact on seed-set in the subalpine lupines (Breedlove and Ehrlich, 1968). In the summers of 1969, 1970 and 1971, an attempt was made further to elucidate the coevolution of plants and their predators by investigating the pattern of G. lygdamus attack on a suite of perennial herbaceous legumes. The studies were done at a series of sites between 8000 and 9500 feet in or adjacent to the Artemisia tridentata Nuttall (sagebrush) association in the upper drainage of the Gunnison River in Gunnison County, Colorado.

Egg censuses and observations of oviposition at these sites have shown Glaucopsyche lygdamus oviposition on the following Leguminosae: Lupinus bakeri Greene, L. jloribundue Greene, L. caudatus Kellog, L. argenteus Pursh, Thermopsis montana Nuttall, Vicia americana Muhlenberg, and Astragalus miser Douglas. Utilization of these plants as oviposition sites was, however, far from uniform. At all sites either a Lupinus species or Thermopsie was by far the most heavily utilized. V icia americana was also commonly used, and laboratory rearings indicated that all of these plants could successfully support larval growth. A single female was observed to go through oviposition behavior twice on Astragalus miser without ovipositing and then to fly to another A. miser plant and lay one egg. No further eggs were found on this species and we are not certain it can be a satisfactory larval foodplant. Table 1 summarizes the patterns of oviposition at a series of sites in 1971. For Lupinus and Thermopsis, eggs per 100 inflorescences are counted. For Vicia, eggs

8 Oecologia (Berl.), Vol. 10

100

D. E. Breedlove and P. R. Ehrlich:

Table 1. Eggs per 100 sampling units

Locality

Dates

L.

L.

L.

L.

T herm- V icia

bakeri cau- argen- !Iori- opeis

datus teus busuius

Gold # 1 VI-22-24 38 133 •
Gold #2 VI-21-27 19 245 56 •
Gold #3 VI-21 40 434 104 +
Gold #3 VI-24 + 680 + 30
Above Gold # 3 VII-2 + 973 +
(N = 30)&
Naked Hills VI-27 3 1
(N = 200)&
Naked Hills Vll-30 21 87 +
Landslide
Jacks Cabin # 1 VI-30 29 + +
Jacks Cabin # 2 VI-26 6 6
Smith Hill VI-25 16 5
- Not present. • Present but rare. + Common but not censused.
& Sample not equal to 100, but data expressed as eggs per 100 inflorescences. per 100 stalks (see below). It is possible to distinguish G. lygdamus eggs from those of all other lycaenids in the same localities by miscroscopic examination.

The pattern of attack on the Lupinus species is related to the pubescence of the plant. Of the four species of Lupinus utilized L. bakeri and L. caudatus have the densest placement of hairs in the oviposition sites, L. bakeri with erect hairs and L. caudatus appressed hairs. In both cases the hairs would prevent oviposition on the substrate. Lupinus arqenteue and L. floribundus are much less densely pubescent, and the hairs are suberect. Thermo-psis has very short, widely spaced hairs. From Table 1 it can be seen that whenever G. lygdamu._~ had a choice it oviposited preferentially on the inflorescences of the least hairy Lupinus present. This pattern, interestingly, is reversed in the closely related Plebejus icarioides Boisduval which oviposits on nonfloral parts and attacks the most hirsute Lupinus preferentially (Downey, 1962). Our unpublished data on P. icarioides support Downey's conclusions.

T'hermopsis montana is strongly preferred as an oviposition site over both of the hairy Lupinus, but does not receive as many eggs as the most favored Lu pinus, L. floribundus. This pattern is supported by ob-

Coevolution: Patterns of Legume Predation by a Lycaenid Butterfly 101

servations where accurate censuses were not possible. For instance at above Gold # 3 L. floribundus was attacked at the highest level yet observed, although the population was so small only 30 inflorescences could be censused. L. bakeri was abundant all around the small colony of L. floribundus (which averaged 9.7 eggs/inflorescence), and yet casual examination of several dozen inflorescences revealed no sign of G. lygdamus attack (the inflorescences were too mature for a comparable census). Similarly L. floribundus at Jacks # 1 was heavily attacked, much more so than L. caudatus at Jacks # 1 or L. bakeri at the nearby Jacks # 2, but the inflorescences were too far along to permit comparable censusing.

Oviposition on Vicia is difficult to compare to Lupinus and Thermopeis, on which counts of eggs per 100 inflorescences are made. On V icia eggs are laid mostly in the tight cluster of immature leaflets of a newly opened leaf bud. Samples are taken by counting eggs on the leaves of 100 Vicia stems which start from ground level. This rough comparison indicates Vicia is less frequently utilized than any of the other plants with the possible exception of L. bakeri,

The selective advantage to the plant of avoiding attack by G. lygdamus suggested by our earlier work (Breedlove and Ehrlich, 1968) was again indicated by experiments in which eggs were removed from one group of plants, and fruit-set on those controls compared with that on plants on which the eggs remained. At Gold Basin # 2 fifty control Thermopsis montana inflorescences from which 51 eggs (all those visible) were removed set fruit from 502 to 593 potential flowers (85%). Fifty inflorescences on which 51 eggs were counted but not removed set fruit from only 421 of 672 potential flowers (63 %). The difference is highly significant (P < < 0.01). A biased sample of 25 inflorescences which had three eggs or more per inflorescence (X =4.6) showed that G. lygdamus can be heavily destructive on 'I'hermopeis, with only 198 of 368 potential flowers actually setting fruit (54 % ).

The heaviest attack detected was on Lupinus jloribundus, At Gold # 3 fifty control inflorescences from which 298 eggs were removed set fruit from 2031 of 2400 potential flowers (85%). In contrast an experimental group of fifty inflorescences on which 695 eggs were left set fruit from only 442 of 2633 potential flowers (17%). The difference may be somewhat exaggerated here since logistic problems forced us to use as controls plants on which relatively few eggs had been laid. Some eggs had already hatched when we started the study and the young larvae are difficult to find and remove without destroying flowers. This basis was probably compensated in part by two factors. First, some larvae probably escaped detection on the controls and destroyed flowers. Second, when 13 eggs or more were allowed to remain on an inflorescence more than

102

D. E. Breedlove and P. R. Ehrlich:

85 % of the flowers on that inflorescence were always destroyed. The mean number of eggs left in the experimental group was 13.9, and 21 inflorescences had more than 13 eggs (14 had 20 or more, the maximum being 44). Thus a sizeable portion of the attack on the experimental group was" overkill".

It seems likely that Glaucopsyche iygdamus is an herbivore that is very often resource-limited. Legume inflorescences with the proper characteristics and at the proper state of development seem to be required for the larvae (an exception to this may exist in the case of Vicia where the pattern of larval feeding in nature is unknown). In some circumstances the resource may be limiting because the egg population far exceeds the capacity of the plant to support an equal larval population. This would be the case in several populations feeding primarily on Lupinus jloribundus.

In other circumstances weather may destroy much or all of the required food resource. Drought at both Gold # 2 and Gold # 1 in 1971 killed many Lupinus inflorescences. All were destroyed at Gold # 1. In both of these localities G. iygdarnus should have no difficulty persisting because of the presence of Thermopsis populations, which were able to mature their flowers successfully, growing along nearby watercourses. Populations of G. iygdamus feeding on Lupinus in drought areas where Thermopsis was not present may well have gone extinct. One large G. iygdamus population feeding on L. bakeri was wiped out in 1969 when a late snow destroyed the lupine inflorescences (Ehrlich et al., 1972, in press), in spite of the presence of Vicia which was not damaged seriously by the snow and might have provided a suitable alternate host. This G. iygdamus population, Naked Hills, had not been firmly reestablished in 1971 in spite of the presence of a thriving popu- 1ation utilizing L. bakeri and L. arqenteus at Naked Hills Landslide one mile away.

Annual plants in variable environments may be thought of as undependable resources which are only present when conditions are proper. But herbivores utilizing such resources have often evolved mechanisms which synchronize their activities with the availability of the resource (cf. Linsley et al., 1964). Those organisms attacking the inflorescences of perennials in such environments face at least equal uncertainty in the frequent aborting of inflorescences in response to a variety of climatic perturbations (Ehrlich et al., 1972, in press). Indeed, one of the great advantages of the perennial habit must be the ability to destroy entire populations of flower-feeding herbivores by sacrificing seed production for a single season-an evolutionary strategy not available to annuals.

The small amount of evidence we have accumulated thus far seems to indicate that Giaucopsyche lygdamus populations may suffer rather

Coevolution: Patterns of Legume Predation by a Lycaenid Butterfly 103

heavily from the attacks of parasites. Predators, on the other hand, probably do not take a heavy toll of the cryptic larvae after they are large enough to emerge from individual flowers and feed exposed. Day to day observation of large larvae in the field shows little evidence of predation. The larvae are often protected by aggressive ants which tend them in return for the secretions of specialized "honey" glands. The evidence points to resource shortage and parasite attack as often being the major factors in population limitation.

Our data raise some interesting questions. Why, for instance, should not G. lygdamu8 make extensive use of Lupinus bakeri at places like Gold # 3 instead of expending its reproductive effort on the less abundant L. floribundus? Why are any eggs laid on Vicia when lupines or Thermo-psis are present? Is the failure of the weedy L. floribundu8 to penetrate sagebrush areas in any way related to its susceptibility to G. lygdamus attack (perhaps it exists as a fugitive species) ? What stimuli determine choice of oviposition plant in G. lygdamus, and are there genetic differences among populations in response to these stimuli? Are there significant biochemical or other differences among different populations of the same plants?

Answers to these and other questions must await the results of investigation now under way. It is already clear, however, that patterns of food plant utilization by the butterflies and defensive strategies of the plants may be extremely complex and that determining the amount and dependability of a food resource for a given herbivore in a given area can be very difficult.

Acknowledgements. We thank Anne H. Ehrlich, Lisa M. Ehrlich, Sarah Gage, John Kipping and Katherine Kipping for help with various aspects of this work. David B. Dunn, Department of Botany, Univ. of Missouri, has been kind enough to identify the lupine species. The field work reported herein was done at the Rocky Mountain Biological Laboratory, Crested Butte, Colorado. The use of their facilities is gratefully acknowledged. Supported by NSF grants GB-19686 and GB-22853, and a grant from the Ford Foundation.

References

Breedlove, D. E., Ehrlich, P. R.: Plant-herbivore coevolution: lupines and lycaenids.

Science 162, 671-672 (1968).

Downey, J. C.: Host-plant relations as data for butterfly classification. Syst. Zool. 11, 150-159 (1962).

Ehrlich, P. R.: Coevolution and the biology of communities. In: Biochemical coevolution, ed. K. L. Chambers, p. 1-11. Oregon: Corvallis 1970.

Ehrlich, P. R., Breedlove, D. E., Brussard, P. F., Sharp, M. A.: Weather and the regulation of subalpine populations. Ecology 53, 243-247 (1972).

Ehrlich, P. R., Raven. P. H.: Butterflies and plants: A study in co-evolution.

Evolution 18, 586-608 (1965).

104 D. E. Breedlove et ai.: Coevolution: Patterns of Legume Predation

Janzen, D. H.: Coevolution of mutualism between ants and acacias in Central America. Evolution 20, 249-275 (1966).

Janzen, D. H.: Seed-eaters versus seed size, number, toxicity and dispersal. Evolution 23, 1-27 (1969).

Janzen, D. H.: Herbivores and the number of tree species in tropical forests. Amer.

Naturalist 104, 501-528 (1970) .

. Janzen, D. H.: Escape of juvenile Dioclea meqacarpa (Leguminosae) vines from predators in a deciduous tropical forest. Amer. Naturalist 10ii, 97-112 (1971).

Linsley, E. G., MacSwain, J. W., Raven, P. H.: Comparative behavior of boos and Onagraceae. III. Oenothera boos of the Mojave Desert, California. U. Calif. Pub. Ent. 33, 59-97 (1964).

Dr. Dennis E. Breedlove Department of Botany California Academy of Sciences San Francisco, California 94118 U.S.A.

Dr. Paul R. Ehrlich

Department of Biological Sciences Stanford University

Stanford, California 94305

U.S.A.