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FACTORS INFLUENCING POPULATION DYNAMICS AND STABILITY WITHIN A THREE TROPHIC LEVEL SYSTEM: MESQUITE SEEDS, BRUCHID BEETLES, AND PARASITIC HYMENOPTERA by Robert A. Kistler . A Dissertation Submitted in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy in Zoology Northern Arizona University May 1985 ABSTRACT FACTORS INFLUENCING POPULATION DYNAMICS AND STABILITY WITHIN A THREE TROPHIC LEVEL SYSTEM: MESQUITE SEEDS, BRUCHID BEETLES, AND PARASITIC HYMENOPTERA Robert A. Ktstler A three trophic level ecosystem consisting of the seeds of velvet mesquite (Prosopis velutina: Leguminosae), four species of seed beetles (Coleoptera: Bruchidae) and a complex guild of more than 17 species of parasitoids (Hymenoptera) was studied in the Verde Valley in central Arizona. The phenology of marked trees in six populations of mesquite was monitored and seed pods were collected from these trees every two weeks from 1981 through 1983. The insects .in the seeds were reared in the laboratory. Laboratory and field experiments examined the physiological ecology of the bruchids and parasitoids and the capabilities of these two guilds to regulate populations of their respective hosts. Individual mesquites produced a large pod crop, consisting of high quality seeds, every two years at the most. Apparent energy and nutrient limitations either inhibited pod production totally in alternate years or limited seed production severely if pods were produced. Along with a lack of synchrony in reproduction, this created a tremendous heterogeneity, in the number and ease of location, of good seeds which could be used by the bruchids. This heterogeneity in space and time combined to severely limit the impact of the seed predators on the seed populations. Key factor analysis of ovule and seed mortality across the six populations indicated that pre-predation ovule mortality accounted for most of the decrease in potential reproductive output, while seed predators were not a significant key factor. The bruchid species were differentially adapted to the extreme temp~ratures experienced in the field, with Algarobius prosopis being most tolerant to temperature variation. Similarly, !· prosopis was most adapted, via a modified oviposition strategy, to attack by trichogrammatid egg parasitoids. The other three bruchid species, Mimosestes amicus, Mimosestes protractus and Neltumius arizonensis were the less successful members of the seed predator guild. The diverse community of larval and egg parasitoids possessed a strong capability to regulate populations of the second trophic level. Bruchids were not significant in t~is and should exert little or no selective pressure on reproductive strategies of mesquite. system TABLE OF CONTENTS Page ABSTRACT i i PREFACE . vi ACKNOWLEDGMENTS vi i LIST OF TABLES vi i i LIST OF FIGURES • X CHAPTER 1. 2. 3. Genera 1 In trod u c t i on. State of Knowledge: Bruchid-Legume Systems. Literature Cited . . • • • • • • • • • • 0 • 0 • Q Seed Production in Prosopis velutina (Leguminosae): Variability and the cost of Reproduction in a .Desert Phreatophyte • . Introduction Methods . . . Study site • Study methods. Results . . . . . Cost of reproduction . . • . . . . • Variability in reproductive output • Discussion Literature Cited . Reproductive Strategies in Prosopis velutina (Leguminosae) and their Effect on Seed Predation by Bruchid Beetles . . . . . • Introdu.ction . Methods Results F~lower production and mortality. . Non-predation ovule and immature seed mortality . . . . . . . . . Predation related mortality. Variation in seed production and predation by bruchid beetles • • • . • . . . . . i v 1 7 12 18 19 23 23 23 26 29 34 44 53 62 63 65 69 69 71 73 77 CHAPTER Page Key factor analysis: The relative influence of factors on seed survivorship • Discussion Literature Cited • • • . • . . . • • 4. 99 102 108 113 113 114 117 137 154 The Role of the Third Trophic Level in the Mesquite-Bruchid Ecosystem . . . • . • . . . . Introduction . . . . . . . . . Methods Results and Discussion Literature Cited 161 162 163 165 175 General Discussion Literature Cited 177 184 . 6. 87 The Effect of Temperature on Mesquite Bruchids (Coleoptera): Physiological Strategies of a Guild of Seed Predators Introduction . • . . Methods • • • . Field studies • Laboratory studies Results . • • • • . Discussion Literature Cited ....... 5. 82 v PREFACE 11 For the world of science and evolution is far more nameless and elusive and like a dream than the world of poetry or religion; since in the latter, images and ideas remain themselves eternally, while it is the whole idea of evolution that identities melt into each other as they do in a ni ghtmare 11 • G. K. Chesterton The Ball and The Cross 11 lt is interesting to contemplate an entangled bank, clothed with many plants of many kinds,with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp earth, and to reflect that these elaborately constructed forms, so different from each other, and dependent on each other in so complex a manner, have all been produced by laws acting around us 11 • Charles Darwin The Origin of Species vi ---------------------------------------------------------------------------, ACKNOWLEDGMENTS I thank Russell Balda, Dean Blinn, Wally Covington, C.D. Johnson, Peter Price, and Con Slobodchikoff for their help and support as members of my research committee. I thank C.D. Johnson for providing research space and materials and for identifying the bruchids in this study. I would especially like to thank Peter Price for taking the time to listen, for acting as an exemplary ecologist, and for reviewing not only my dissertation, but also many other manuscripts. I thank all of my graduate school colleagues, who through interaction and discussion have been a major part of my graduate training. I especially thank Doug Hay, Martin Hetz, Kris Mobley, Bob Graybosch, and Ken Paige. I thank the Department of Chemistry, Northern Arizona University, for the generous loan of their Gilson respirometer, which made a large part of this work possible. I dedicate this dissertation to my wife, Candi, my daughter, Kareena, and my God, without whose support, patience and guidance this all would not have been possible. vii LIST OF TABLES Table 2-1. Page Descriptive data on the. six populations of Prosopis velutina examined in the study. . . . . . . . . . . 24 Early reproductive structures in P. velutina at six sites in 1983 . . . . . . . . . . -. . . . . 30 2-3. Reproductive costs for tree #1 at site 1 in 1983. . . 32 2-4. Pod and seed production and abortion in P. velutina . 35 2-5. Two-way analysis of variance of total seeds and total good seeds by year and site . . . . . . . 36 2-6. Pod and seed data for e1ach site by year . . 37 3-1. The number of inflorescences produced and setting fruit in six populations of f .. velutina in 1983 . . . . 70 Seed mortality in!:_. ve,lutina in six sites over three years . . . . . . . . . . . . . . . . . . . . . . . . 72 Stage of ovule or seed attacked by Lepidoptera and Bruch i dae in P. ve 1uti na. . . . . . . . . . . . . . 75 Two-way analysis of variance of bruchid and moth emergence by site and year. . . . . . . . . . . . . . . 76 Correlation coefficients of the number of bruchids emerging from seed pods with various factors. . . . 78 Key factor analysis of flower, ovule, and seed mortality in six populations of P. velutina over a three year period . . . . . . . . - : - · . . . . . . . . . . . . . . . 83 2-2. 3-2. 3-3. 3-4. 3-5. 3-6. 4-1. 4-2. Relative abundance of b:ruchids in the mesquite seedpredator guild. . . . . . . . . . . . . . . . . Numbers of bruchids eme,rged from 30 pod !:_. velutin.a over a three year period. . sample~ 119 of 120 4-3. Internal temperatures of mesquite pods. . . . . 123 4-4. Temperature constants for bruchids that attack seeds of P. velutina. . . . . . . . . . . . . . . . . . . . . 135 Adult weights and percent water for the four members of the mesquite bruchid guild . . . . . . . . . . . . 138 4-5. vi i i Table Page 4-6. Egg weights and percent water for the members of the mesquite bruchid guild . . . . . . . . . . . . . 5-1. Parasitoids of the mesquite seed predator guild . . . . . . 170 i X . 139 LIST OF FIGURES Figure Page 1-1. The mesquite-seed predator-parasitoid food web . . . . . 11 2-1. Phenology of reproduction in six populations of Prosopis velutina over three years. . . 27 2-2. Climatic data for 1981 to 1983 for the study sites . . . 28 2-3. Parental investment in terms of biomass and water in various stages of flowering and fruiting in f.. velutina. 31 Cost of pod production in terms of dark respiration and biomass of pods in .!:.:_ _glandulosa . . . . . . . . . . 33 Relationship of pod production with tree size in f.. ve 1uti na . . . . . . . . . . . . . . . . . . . . . 38 2-6. Pod production in f.. ve!l utina over three years 40 2-7. The number of pods produced per unit volume of tree foliage as a function of tree size . . . . . . 42 2-8. Reproductive gain as a function of reproductive investment in P. velutina. . . . . . . . . . . . . . . . . 43 The percent of seeds killed by bruchids in relation to the total number of :good seeds produced per tree. 79 The proportion of seeds killed by bruchids as a function of the proportion of good seeds produced per tree . . . . . . . . . . . . . . . . . . . . 81 Key factor analysis of reproductive mortality in five populations of f.. velutina in 1983 . . . . . . . . 85 Key factor analysis of post-flowering reproductive mortality in f.. velutina . . . . . . 86 2-4. 2-5. 3-1. 3-2. 3-3. 3-4. 4-1. Temporal patterns of climate and the bruchid and tree populations. . . . . . . . . . . . . . . . . . . 118 4-2. Diurnal temperature variation in a mesquite tree . . 122 4-3. The relationship of metabolic rate and temperature for adults of the mesquite seed beetle guild . . . . . 125 The relationship of metabolic rate and temperature for larvae of the mesquite seed beetle guild . . . . . 126 4-4. X Figure 4-5. 4-6. 4-7. Page Relationship of metaboiic rate with dry weight for 11 species of Bruchidae . . . . . . . . . . . . . . . 12 7 Relationship of fecundiity and temperature for the mesquite bruchid guild . . . . . . . . . . . . . . . 130 Longevity"- temperature relationships for the adult bruch ids . . . . . . . . . . . . . . . . . . . . . . . 131 4-8. Weekly fecundity over the lifespan of the bruchids . . . . 132 4-9. Developmental rates and times of the egg and larvalpupal stages at the experimental temperatures. . . . . 134 Relative survivorship of larve of the three species of bruchids . . . . . . . . . . . . . . . . . . . . . . 136 Relation between wet weight and dry weight of adult bruchids...................... 140 4-10. 4-11. 5-1. Population dynamics of the larval parasitoids and their host bruchids . . . . . . . . . . . . . . . . . . . . . . . 166 5-2. Population dynamics of the bruchids, larval parasitoids, and egg parasitoids in the mesquite ecosystem for 1983 at site 1. . . . . . . . . . . . . . . . . . 167 5-3. The relationship between egg densities in the field and the number of bruchid eggs parasitized . . . 169 The subdivision of the larval bruchids by their parasitoids. . . . . . . . . . . . . . . . . 171 Differential rates of parasitism of the eggs of three species of bruchids. . . . . . . . . . . . . . . . . . 172 5-4. 5-5. xi CHAPTER 1 GENERAL INTRODUCTION 1 2 Our understanding and knowledge of ecological communities has recently been questioned. Lawton and Strong (1980) reviewed work on insect communities and concluded that competition may not explain all or most of the patterns of organization seen in these communities. Similarly Wiens (1977) and Connell (1980) questioned the role of competition in the dynamics of populations within other animal communities. Price et al. (1980) stress that most knowledge of ecological communities is limited to at most two trophic levels, with a striking void of information on the roles played by predators and parasitoids in communities, despite the fact that all three major trophic levels appear to be tightly linked. In order to address these problems it is necessary to examine ecological communities as a unit to elucidate those factors which regulate the dynamics of the component species. Lawton and Strong specifically propose that a climate which is harsh and variable, host plant phenology, patchiness of resources and natural enemies must all be considered to understand community dynamics. This research examines a three trophic level system in an attempt to synthesize a comprehensive picture of _the dynamics of the system and those factors that are important in the dynamics, regulation and stability of each of the component trophic levels. Regulation of populations has been divided into two major types. Andrewartha and Birch (1954) through their 3 work on Thrips imaginis found four climatic factors that could explain 73% of the population variation. Morris (1969) explained much of the variation in northern populations of the fall web worm (Hyphantria cunea) by temperatures in the fall feeding period. I have demonstrated that temperature may greatly affect fecundity, development and physiology of a set of desert beetles in the family Bruchidae (Kistler 1982). The above examples demonstrate that abiotic factors, especially in harsh, variable environments, do have a large impact on insect populations. Biotic factors also may regulate populations, through food limitation (food quality or amount), competition within a trophic level, predation between trophic levels and through coevolution both within and between trophic levels. The quantity of food is usually not limiting for herbivorous insects although food quality and accessibility are largely variable as a result of defensive mechanisms of plants. However, food quantities may be directly limiting to higher trophic levels. Mechanical defenses of plants may affect both herbivorous and granivorous insects and their predators. Seed pod morphology (thickness and hardness) and behavior (gum production, indehiscence) may negatively affect both bruchid beetles that feed in the seeds contained within the pod (Center and Johnson 1974, Johnson 1981a) and the parasitoids that oviposit on the larvae developing within the seeds (Price et al. 1980). Seed coats may also 4 be a barrier to the entry of bruchid larvae and to oviposition by parasitoids. Stator sordidus and S. Two species of bruchid beetles, limbatus, could not enter intact seeds of Cercidium floridum or Parkinsonia aculeata until after I had removed the seed coat (Kistler unpub. data, Johnson 1981b). Defensive chemicals produced by plants may also affect the dynamics of higher trophic levels. The optimal defense theory that has been developed by Feeny (1976), Rhoades and Cates (1976), and Rhoades (1979) predicts that plants should be protected by chemicals that either make the entire plant (or parts of the plant that are most important) inedible or difficult and expensive to digest. b~ well protected. Seeds especially should Janzen (1977) showed that Callosobruchus maculatus (F.) larvae die after attempting to eat many species of non-host seeds. The mean developmental time of Stator sordidus is lengthened significantly on certain non-host seeds (Johnson 1981b). These chemical defenses may in turn be detoxified by insects (Rosenthal 1982), and even used as a defense against predators and parasitoids (Cambell and Duffey 1979). The plant, therefore, has an array of potential defenses against attack, which either may decrease attack directly by mechanisms like those above or indirectly by association with other plants in a "defensive guild" (Atsatt and O'Dowd 1976). However, each strategy of defense also may have a negative impact on predators and parasitoids of the plant-attacking insects. The optimal strategy must 5 invariably be a compromise solution yielding the highest possible protection from attack over both ecological and evolutionary time. Such plant defenses may be stabilizing or may result in fluctuations within insect populations (Haukioja 1980). Predators and parasitoids may also regulate populations of insects within a community. The selective pressure placed upon insects by their enemies may result in one of three potential outcomes. Enemies may (1) strongly suppress insect populations, leading to local extinctions; (2) coevolve ~ith their prey or (3) result in selection for "enemy free space" (Lawton 1978) in prey populations. Suppression of prey by enemies may either be stabilizing or destabilizing within a community. Paine (1966) demonstrated that predators are capable of regulating community composition and dynamics. Hassell (1978) reviewed the effects of enemies on insect populations and factors that determine when relationships will be stabilizing or destabilizing. Utida (1957) and Fujii (1983) have shown that two non-coevolved parasitoids may either stabilize or destabilize their host bruchid populations. The destabilizing parasitoid, Heterospilus prosopidis Viereck (Hymenoptera:Braconidae) has a very high searching efficiency and causes violent oscillations of the host population, resulting in local extinction of the parasitoid. In contrast, Anisopteromalus calandrae Howard (Hymenoptera:Pteromalidae) stabilizes the host population 6 resulting in stable coexistence. I examined some major population parameters of these host and parasitoid populations and concluded that the major factor responsible for these different responses was the different functional responses of the two parasitoids (Kistler 1979, 1985). Coevolution of enemies with their prey has been conceptually well developed, but its importance in natural systems is still largely conjectural. Pimental (1968) and Pimental et al. (1978) found that in a laboratory system of the house fly (Musca domestica) and its parasitoid (Nasonia vitripennis Walker) the fecundity of the parasitoids decreased after a few generations. They concluded that coevolution in host-parasitoid systems may result in selection for intermediate rates of increase in the parasitoid populations. This phenomenon was also demonstrated in the rabbit-myxomatosis virus introductions in Australia and so is possible in semi-natural systems (Fenner 1971). Similarly, coevolution has been thought to be prominent in legume-bruchid systems (Janzen 1969, Center and Johnson 1974). This work addresses the role of abiotic factors, competition, predation, stability and coevolution and their effects on and importance in ecological communities by a comprehensive examination of a natural three trophic level ecosystem. An examination of a simple, natural, three trophic level system should provide some possible answers to questions about community dynamics by linking together for 7 one system all the potential interactions and ecological and evolutionary responses of all three trophic levels. Some potential interactions that might be better understood by such a comprehensive approach are: the responses of the plant to its enemies and to the predators of these enemies, the responses of the plant eaters to the defenses of the plant and to its enemies, and the responses of the parasitoids to the defenses of the herbivores, and to the attraction mechanisms of the plant. State of Knowledge: Bruchid-Legume Systems A large store of information is available on interactions between bruchid beetles and their host seeds. This provides an excellent conceptual base for two of the major trophic levels of the legume-bruchid-parasitoid community examined in this study. Most of these data and resulting hypotheses have resulted from the work of D.H. Janzen, C.D. Johnson, and their students. Seeds are the most important plant part in that they are directly related to the reproductive fitness of the plant. The parent tree should be under strong selection to evolve the best strategy to produce the most viable ~eeds and seedlings at the least possible cost (Rhoades 1979). At least four hypotheses have been proposed as to strategies used by plants to protect their seeds. Plants may: (1) produce many small seeds in an.effort to satiate the local seed predators (Janzen 1969), (2) produce relatively fewer, 8 more well protected seeds (increased seed size, increased chemical protection, or increased mechanical protection, Janzen 1969, Center and Johnson 1974, Rosenthal 1982), (3) produce seeds that are attractive to dispersal agents which dis'perse seeds away from the parent plant (Janzen 1972, 1976, Janzen and Martin 1981, Lamprey and Halevy 1974), or (4) produce such a wide mosaic of seeds and seed pods both within one tree and in the tree population that seed predators are unable to attack most seeds (Whitham and Slobodchikoff 1981). These strategies may either be employed by different plants or several strategies may be used by the same plant or species of plant. Seed-feeding insects such as bruchid beetles should in turn be under intense selection to circumvent ·any defensive mechanism of their host plants. For the most part, this selection appears to have resulted in increased specificity in the Bruchidae. The majority of bruchids are extremely host specific, resulting from a hypothesized coevolution of specific bruchids with specific host plants (Johnson 1981a). This specificity can result from chemical coevolution with the seeds of a given plant (Rosenthal 1982) or from a coevolution with a specific seed dispersal strategy. Johnson (1981a) described three guilds of bruchids feeding on legume seeds. One guild attacked only seeds contained in indehiscent pods on the parent tree, while another guild attacked only seeds from partially dehiscent pods and a 9 third only attacked seeds from dehiscent pods which had been dispersed away from the parent tree. Some bruchids may alternately be extreme generalists with a high fecundity and may attempt to satiate the legum~ community with eggs, some subset of which will survive (e.g., Stator limbatus, Kistler 1982). The strategy chosen by a given bruchid may be due in large part to physiological constraints on the bruchids or to selection for enemy-free space. Parasitoids are the third major trophic level component in legume-bruchid systems. Comparatively little is known about their significance in these systems. Center (1974) and Center and Johnson (1976) list many parasites in most of the legume-bruchid systems that they have examined in Arizona, and these may have a significant impact on both the bruchid populations and on the host plants and their appropriate evolutionary strategies. There is an extensive theoretical and descriptive data base on bruchid-legume systems and this makes it feasible and desirable to examine these communities. These communities are simple, in that they consist of: (1) a quantifiable seed resource, which is also a potential measure of the plant's fitness, (2) seed attacking bruchid beetles, which develop as larvae inside the seeds and are thus also easily quantifiable, and (3) the parasitoids which develop on the bruchid larvae within the seeds. The large data base on the bruchid-legume interactions will make the 10 task of adding the third trophic level much simpler and will prove helpful in understanding the function of the parasitoids in the system. Five major questions were addressed in the examination of a three trophic level desert ecosystem in this study (Fig. 1-1). 1). What factors regulate seed production prior to seed dispersal and seed predation? 2). Do bruchid beetles exert significant selective pressure on reproductive strategies of the host plant? 3). Does the tree exert any selective pressure or regulatory action on the populations of its seed predators? 4). What factors regulate and organize the complex community of seed predators? 5). Are the parasitoids, which make up the third trophic level, important in the regulation or organization of the seed predator communities or alternately are the parasitoids an important component of the plant's defensive strategies against seed predators? 'lliiRD TROPHIC Mmi EGG EARLY lliSTAR lEVEL PARASI10Ill3 PARASI10Ill3 PARASI10ID3 . (5) SECX>ND (1?) LATE lliSTAR PARASI10Ill3 (1+) TROPHIC lEVEL MISC. (4) BRUCH IDS GENERALISTS MICROLEPIDOPTERA SPECIALISTS MIMOSESTES N1ICUS ALGAROBIUS PROSOPIS NELTUMIUS ARIZONENSIS MIMOSESTES PROTRACTUS FIRST TROPHIC AL'IERNA1E lEVEL HOST I MESQUI'IE SEEll3 SEEll3 Fig. 1-1. The mesquite-seed predator-parasitoid system. The numbers in parentheses under the parasitoids indicate the minimum number of species. Miscellaneous parasitoids includes all those species that attack either all larval stages or for which the stage of attack is uknown. ....... ....... 12 LITERATURE CITED Andrewartha, H.G. and L.C. Birch. 1954. The distribution and abundance of animals. Chicago, University of Chicago Press. Atsatt, P.R. and D.J. O'Dowd. 1976. Plant defense guilds. Science 193:24-29. Cambell, B.C. and S.S. Duffey. 1979. Tomatine and parasitic wasps: Potential incompatibility of plant antibiosis with biological control. Science 205:700-702. Center, T.D. 1974. A survey of some legume seed-feeding insects of Northern Arizona with notes on the life histories of the Bruchidae (Coleoptera). Unpublished .M.S. Thesis, Northern Arizona University, Flagstaff, Arizona, 157pp. Center, T.D. and C.D. Johnson 1974. Coevolution of some seed beetles (Coleoptera: Bruchidae) and their hosts. Ecology 55:1096-1103. Center, T.D. and C.D. Johnson 1976. Host plants and parasites of some Arizona seed-feeding insects. Ann. Entomol. Soc. Amer. 69:195-200. Connell, J.H. 1980. Diversity and the coevolution of competitors, or the ghost of competition past. 35:131-138. Oikos 13 Feeny, R. 1976. Plant apparency and chemical defense. pp. 1-39, In; J. Wallace and R. Mansell (eds.) Biochemical interactions between plants and insects. Recent Adv. in Phytochem. 10:1-40. Fenner, F. 1971. Evolution in action: Myxomatosis in the Australian wild rabbit. In: A. Kramer (ed.) Topics in the study of life. The Bio Source Book. New York, Harper and Row. Fujii, K. 1983. Resource dependent stability in an experimental laboratory resource-herbivore-carnivore system. Res. Popul. Ecol. Suppl. 3:15-26. Hassell, M.P. 1978. The dynamics of arthropod predator-prey systems. Princeton Univ. Press, Princeton, New Jersey. Haukioja, E. 1980. On the role of plant defenses in the fluctuation of herbivore populations. Oikos 35:202-213. Janzen, D.H. 1969. Seed-eaters versus seed size, number, dispersal and toxicity. Ecology 23:1-27. Janzen, D.H. 1972. Escape in space by Sterculia apetala seeds from the bug Dysdercus fasciatus in a Costa Rican deciduous forest. Ecology 53:350-364. 14 Janzen, D.H. 1975. Interactions of seeds and their insect predators I parasitoids in a tropical deciduous forest. pp. 154-186, In: P. Price (ed.) Evolutionary strategies of parasitic insects and mites. Janzen, D.H. 1977. How southern cowpea weevil larvae (Bruchidae: Callosobruchus maculatus) die on nonhost seeds. Ecology 58:921-927. Janzen, D.H. and P.S. Martin 1981. Neotropical anachronisms: The fruit the Gomphotheres ate. Science 215:19-27. Johnson, C.D. 1981a. Interactions between bruchid (Coleoptera) feeding guilds and behavioral patterns of the Leguminosae. Environ. Entomol. 10:249-253. Johnson, C.D. 1981b. Host preferences of Stator in non-host seeds. Environ. Entomol. 10:857-863. Kistler, R.A. 1979. A simple host-parasitoid system: An examination of factors contributing to stability. Unpublished M.S. Thesis, Purdue University, West Lafayette, Indiana. Kistler, R.A. 1982. Effects of temperature on six species of seed beetles (Coleoptera: Bruchidae: an ecological perspective. Ann. Entomol. Soc. Amer. 75:266-271. 15 Kistler, R.A. 1985. Host age structure and parasitism in a laboratory system of two hymenopterous parasitoids and larvae of Zabrotes subfasciatus (Coleoptera: Bruchidae). Environ. Entomol. in press. Lamprey, H.F. and 0. Halevy. 1974. Interaction between Acacia bruchid seed beetles and large herbivores. Afr. Wildl. J. 12:81-85. Lawton, J.H. 1978. Host plant influences on insect diversity: the effects of space and time. L.A. Mound and N. Waloff, (eds.) pp. 105-125, In: Diversity of insect faunas, Oxford, Blackwell Scientific. Lawton, J.H. and D.R. Strong. ·1981. Community patterns and competition in foiivorous insects. Am. Nat. 118:317-338. Mares, M.A., F.A. Enders, J.M. Kingsolver, J.L. Neff, and B.B. Simpson. 1977. plants and animals. Prosopis as a niche component of pp. 123-149, In: B.B. Simpson (ed. ). Mesquite, its biology in two desert ecosystems. Dowden, Hutchinson and Ross, Stroudsburg, PA. Morris, R.F. 1969. Approaches to the study of population dynamics. pp. 9-28, In: W.E. Waters (ed.) Forest insect population dynamics, USDA Forest Serv. Res. Paper, NE-125. Paine, R.T. 1966. Food web complexity and species diversity. Am. Nat.100:65-75. 16 Pimental, D. 1968. Population regulation and genetic feedback. Science 159:1432-1437. Pimental, D., S.A. Levin and D. Olson 1978. Coevolution and the stability of exploiter-victim systems. Am. Nat. 112:119-126. Price, P.W., C.E. Bouton, P. Bross, B.A. McPheron, J.W. Thompson, and A.E. Weis. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41-65. Rhoades, D.F. 1979. Evolution of plant chemical defense against herbivores. Janzen (eds.) pp. 3-54, In:· G.A. Rosenthal and D.H. Herbivores, their interaction with secondary plant metabolites. Academic Press, New York. Rhoades D.F. and R.G. Cates. 1976. Toward a general theory of plant antiherbivore chemistry. Recent Adv. Phytochem. 10:168-213. Rosenthal, G.A. 1982. L-Canavanine, a dietary nitrogen source for the seed predator Caryedes brasilensis (Bruchidae). Sctence 217:353-355. Utida, S. 1957. Cyclic fluctuations of population density intrinsic to the host-parasite system. Ecology 38:442-449. 17 Wiens, J.A. 1977. On competition and variable environments. Amer. Sci. 165:590-597. Whitham, T.G. and C.N. Slobodchikoff. 1981. Evolution by individuals, plant-herbivore interaction and mosaics of genetic variability: the adaptive significance of somatic mutations in plants. Oecologia 49:287-292. CHAPTER 2 Seed Production in Prosopis velutina (Leguminosae): Variability and the Cost of Reproduction in a Desert Phreatophyte 18 19 INTRODUCTION Reproductive output of a plant species may vary considerably both spatially and temporally. This within and between population variation results from a multitude of factors that influence the plant on both ecological and evolutionary time scales. Thus, a major component of variation in plant populations is a result of past and present selective forces that have shaped the current gene pool for each species. However, evidence for actual genetic variability is lacking for many plant populations (Willson 1983, Solbrig and Bawa 1975). Most evidence for variation in populations comes from studies of phenotypic variation, for which the adaptive significance is speculative. Variations in timing of budbreak, leafing, and flowering are common both between and within species although the adaptive significance of such variation is at present uncertain (Lechowicz 1984). Studies that address reproductive adapatations and variability are less ambiguous since the adaptive significance of reproduction is clearer. The individual plant or species that places a larger proportion of fit seeds into the overall seed pool will have more of its genes represented in future generations. Each species of plant has a distinct set of adaptations to achieve maximal representation in the overall seed pool. Timing of reproduction (Augspurger 1981, Janzen 1967), pollination 20 mechanisms (Paige and Whitham 1985, Pyke 1978 ), the number and size of seed produced (Janzen 1969, Harper et al. 1970), defense mechanisms (Janzen 1969, Bell 1978) and adaptations for dispersal (Smith 1975, Janzen and Martin 1981, Janzen 1972) as well as many other factors are all important parts of a species• reproductive strategy (Willson 1983, Schaffer and Gadgil 1975). Within a species, variation in reproduction will have its greatest significance, for it is with other conspecifics, with the same general life history that a given plant must compete most strongly for the same nutrients and germination sites. Each individual plant controls to some extent the quality and quantity of seeds that it can produce via selective abortion of flowers, fruits, and ovules, based upon the resources available for reproduction within that individual (Stephenson 1981). By this method a plant can regulate the amount of energy and nutrients it expends per unit of time to produce an optimal number of seeds. The plant may regulate the genetic quality of those seeds by aborting less fit seeds and flowers in some selective process and provide more parental care to a select number of remaining offspring. For this reason the numerical aspects of seed production (flower, fruit, and seed numbers) tend to vary a great deal more than such factors as seed size, which is constrained by many factors (Harper et al. 1970, Willson 1983). 21 A plant that is optimal for an examination of the adaptive significance of variability in reproduction is the desert phreatophyte Prosopis velutina Wooten (velvet mesquite). P. velutina is a woody legume in the subfamily Mimosoideae, section Algarobia. It has been extensively studied because of its status as a pest plant of range lands in arid habitats such as the desert Southwest (Simpson 1977) and its food, fuelwood and crop potential for arid lands (Felker 1979). Variability in Prosopis is extreme. Morphologically there are three distinctly different forms, single stem~ed, many stemmed erect and decumbent running bush, all of which may be found in a single species (Meyer et al. 1971) or even in the offspring of a single plant (Felker 1979, Felker et al. 1981). Budbreak varies within and between populations (McMillan and Peacock 1964). Growth rates vary significantly between populations, species, offspring of the same plant and even within clones (Felker et al. 1981). Flowering phenology varies from year to year, dependent mainly upon temperature, but it also varies significantly within a population both within and between years (Glendening and Paulsen 1955). Fruit and flower production varies considerably from year to year and from population to population (Glendening and Paulsen 1955, Meyer et al. 1971, Dafni and Negbi 1980). Most populations produce fruits in alternate years, but even this is highly variable (Felker et al. 1984). Genetic variability is high in this 22 self-incompatible, obligately outcrossing genus (Solbrig and Bawa 1975, Simon 1979). Pod and seed composition within one population may vary considerably (e.g., sucrose content of pods varies from 13-36%; Felker 1979, Werker et al. 1973). Most seeds g~rminate in one to five years but some may still be viable after 10 years in the soil (Meyer and Bovey 1982, Tschirley and Martin 1960, Dafni and Negbi 1978). Some of this variation in mesquite is thought to be a result of adaptation to a harsh desert environment, where nitrogen (Shearer et al. 1983), water (Nilsen et al. 1983) and temperature (Dafni and Negbi 1980) are all factors limiting growth and reproduction. This study examines the seasonal phenology of seed production and the cost of and variability in pre-predation and pre-dispersal seed production within and between six populations of velvet mesquite from 1981 to 1983. Reproductive costs and outputs were monitored for these three years in each population in an effort to document the range and extent of variability within and between these populations. A high level of variability could be a result of adaptations to a variable abiotic environment or could be an adaptive mechanism to reduce the impact of seed predators on reproductive output. This chapter documents the variability found in these six populations and addresses the first possibility. The possible effects of variation on populations of seed predators are addressed in chapter 3. 23 METHODS Study Site The study was conducted from March, 1981 through March, 1984 in the Verde River Valley in central Arizona, USA. The Verde Valley consists of upper Sonoran Desert scrub and desert grassland vegetation (Lowe 1964). The major plant species are Prosopis velutina, Acacia greggii Gray, Larrea tridentata (DC.) Coville and various grasses. The majority of the valley has been intensively grazed by cattle. Six populations of mesquite were chosen within an 870 km 2 area. Only discrete populations were chosen and all were isolated from other populations. A general description of the six study sites is presented in Table 2-1. Study Methods Initially five trees were selected from each site, but as the study progressed more trees were selected at most sites to gain a representative sampling of reproductive variability at each site. The height, cover, distance to the first and second nearest neighbors, amount of leaf litter, vegetation under and between the trees, and the distance to the closest surface water source (if any), were all recorded for each tree. Each site was visited every 10 to 14 days from April through November. The proportion of sample trees with leaves, flowers, or pods, the phenological state of each Table 2-1. Descriptive data on the six populations of Prosopis velutina examined in the study. Number of trees is the number of trees studied at each site, tree density is an estimate of the number of trees per site, and rank population size ranks the sites by the number of trees per site. SITE No. LOCATION! LATITUDE ALTITUDE NEAREST TREES (m) RANGE TNSHIP 0 I TOWN 12 14 5E 34 38 45 1036 McGuireville TREE SIZE X ~ SE 58.9±20.3 2 7 14 5E 34 36 50 1021 Montezuma Castle 37.2±22.1 Na.tional Monument 3 11 13 5E 34 31 00 1006 9.6 km SE of Camp Verde 4 10 13 5E 34 31 50 991 5 10S2 13 11N 2 4E 34 33 15 6 12 3E 34 47 00 16 TREE RANK SITE DESCRIPTION DENSITY POPN MAJOR PLANTS HABITAT TYPE #/Ha SIZE 480 3 Prosop1s-veTUtlna near riparian Mimosa biuncifera (Dry Beaver Creek) Acacia ~reg~i i ChTTQps1s l1nearis 64 6 Prosopis velutina Larrea tridentata dry wash 22.4! 3.1 119 5 Prosopis velutina Acacia constricta Chilopsis linearis near riparian (West Clear Creek) 8.0 km SE of Camp Verde 13.6! 6.9 337 2 Prosopis velutina Larrea tridentata flood plain 975 3.2 km SW of Camp Verde 21.4± 4.5 670 1 Prosopis velutina Chilopsis linearis dry wash (Copper Canyon) 1012 4.8 km N of Clarkdale 127.3~ 3.3 158 4 Prosopis velutina Populus fremontii Tamarix pentandra 1Location is based on the legal description of the property (Range and Township; E =east). 2N- Northern Population S- Southern Population Riparian-roadside Verde River N +:> 25 tree, the number and stage of inflorescences (racemes) per branch and the number and stage of fruits (a linear legume pod, 20 em in length) per branch were recorded. Just prior to or after pod fall a random sample of 30 pods was collected from each tree. These pods were placed in an environmental chamber at a thermoperiod of 12 h/30°C and 12 h/25°C for 50 days until all seed-infesting insects had emerged. Ten pods from each tree were then dissected and seeds were classified into three groups: (1) seeds that appeared to be healthy, (2) seeds that started development but failed to completely develop, and (3) seeds that showed no development at all (possibly unfertilized ovules). The healthy seeds were weighed to the nearest 0.01 mg after being oven dried at 60°C for 48 hours. For all 30 pods of each sample, pod length, number of seeds per pod, and number of seeds damaged by herbivorous insects (mainly Hemipterans, that suck the seed fluids - Smith and Ueckert 1974, Kingsolver et al. 1977), grazers (that eat the pods and seeds, e.g., Orthopterans), and ovule and seed predators (mainly Lepidoptera:Olethreutidae and Coleoptera: Bruchidae) were recorded. For the remaining undissected 20 pods of each sample, seeds were classified via an external examination of the pods into one of the three seed classes. Results of this external classification agreed well with the results of the actual dissections and in some cases results were pooled. 26 Levels of pod production and the number of seeds in each seed class were analyzed by one-way analysis of variance and if significant F-values were obtained, Scheffe's multiple range test was utilized to pinpoint significantly different means. Two- and three-factor ANOVA and multiple regression were used to attempt to define which parameters were important determinants of pod and seed production and pre-predation seed mortality. RESULTS The timing of budbreak, flowering and fruiting varied between sites within one year and varied to some extent between years within one site, although the overall pattern usually remained consistent for each population (Fig. 2-1). Within each site there was considerable asynchrony in the phenological timing of adjacent trees, which deviated by a few days or weeks. This variation in phenological timing within and between populations and within and between years can not be readily explained by climatic patterns (Fig. 2-2). Interaction between temperature and rainfall may account for some of the apparent differences between years at each site, but genetic and historical (reproduction in previous year or years) factors may also be important determinants of the within and between site variation. Substantially more inflorescences, flowers and fruits were produced than matured. Most trees in this study 27 100 1983 1981 1983 ,., 1981 I 1981 , '\ I ' . \.: I .. :\ : \ \ oL--£~~~----~~~~~+----+----~--~--~L----~~2-~--~~--~·~·~~----+---~----~--~ 100 3 1983 ,, I .·"\·'·~ 1961 \ ' ' ' ,: \ \ . \: \ ~ ... \• ;,1 ~ "' ,.,..;. ·::~/\., ...... !\ 1961 '! \ \ ........ oL-~~--~i--+~.-~·~--~---+----~--+---~L---+--~----~--~~~~~~~~--~~ A A M MONTH 5 0 N 0 A M J A 5 MONTH Fig. 2-1. Phenology of reproduction in six populat1ons of Prosopis velut1na over three years. Each curve represents the proportion of the population (of trees, flowers, or pods) that were in each state at a given t1me. Arrows indicate the mean bud-break time for the populat1on. Flowenng -----; I11111ature green pods ------; f·1ature dry pods ..•••..• ; Pods on the ground-·-·-·-·-·-· 0 N 0 28 30 u 0 ~ 0 w 2! ~ 0:: :::> § 1~ 0:: t::. 20 ~ w Cl.. ~ w 0 t::. 0 § 1- 10 0 t::. § ~ 0 8 ~ 0 t::. 0 15 0 ~ '' ' ' '\ I' '' 0 I ' z I .. ~ 1Cl.. 0:: Cl.. I /f ~ u 5 w ~~ 0 0 / zY: ' \~,8""""oi: I J F M ~ 0 ' 0 t::. ' 0 t::. Jt + ....., + ~ + <t: 0 -1981 1983 fj =1982 0' ' t::.~ , ' AM 1- ....., 0 6 ', 0 0 '--' J 0 J AS 0 N 0 Fig. 2-2. Climatic data for 1981-1983 from the Beaver Creek Ranger Station near site 1, at Rimrock, Arizona.(data from Vol. 85-87, Climatological Data, Arizona, National Oceanic and Atmospheric Administration! National Climatic Data Center, Asheville, N.C.). The lower figure includes total yearly rainfall and cumulative rainfall for April, May, June, and July. Other data are monthly means. 29 produced hundreds to thousands of inflorescences every year. A large proportion (21 to 85%) of the immature inflorescences were aborted before the flowers had opened (Table 2-2). After flowering, further inflorescences were aborted without ever setting fruit. There was also some abortion of immature fruits, although this factor was not measured. Fruits were not aborted once pod elongation (pods>5cm in length) had begun, although ovule and seed abortion still occurred within a pod. Cost of Reproduction Since such high levels of abortion of individual flowers, entire racemes and early fruit must entail some cost to a plant, samples of immature and mature racemes, and all stages of pods were collected, weighed, dried, and then reweighed to determine the relative cost of these reproductive units in terms of water and biomass investment. It was clear that the relative cost of a raceme or immature pods on a raceme was small, whereas once pod elongation had begun, the parental investment in each fruit increased dramatically (Fig. 2-3). The increase in cost for an entire tree through the immature pod stage was miniscule (54%) when compared to the 4200% increase in cost if each raceme produced only 1.5 pods (the mean number of pods per raceme in this study) (Table 2-3). Data on Prosopis glandulosa in Texas indicate that metabolic costs rapidly decrease after the second week of pod development, when pod elongation 30 Table 2-2. Early reproductive structures in Prosopis velutina at six sites in 1983. # BRANCHES PER TREE SITE TREE 14 15 16 17 18 19 17 34 90 54 28 38 19 22 26 10 33 50 80 +61 +12 160 +15 75 45 90 55 55 40 80 75 30 60 20 nc 35 nc nc 30 31 40 10 27 5 100 30 55 130 30 40 1 2 3 4 5 6 7 18 51 40 35 35 12 30 +81 80 80 55 50 70 nc 150 60 nc 17 nc nc 65 58 40 1 1 20 10 50 1 2 3 4 5 6 7 22 31 20 21 28 23 17 125 135 80 +17 +50 15 40 50 60 45 60 15 25 5 35 0 00 0 0 30 60 43 25 11 10 1 10 55 0 nc nc nc nc nc nc 0 0 1 0 1 1 0 0 0 0 97 62 15 100 13 15 35 26 65 40 4D 75 10 35 40 20 100 100 98 100 98 99 100 100 100 100 1 2 3 4 6 7 7A 8 9 10 12 40 26 29 20 17 18 20 23 70 60 50 18 60 50 +60 +70 70 60 100 0 0 0 0 nc 125 75 nc 53 0 0 0 0 0 0 1 3 0 1 0 100 100 100 100 100 100 100 100 100 99 8 10 20 24 46 90 40 55 70 25 40 15 nc nc nc nc 0 40 1 0 1 9 10 lOA 11 2 3 4 1 2 3 4 5 6 7 8 9 5 6 # MATURE % IMMATURE % RACEMES! # # IMMATURE FLOWERING PODS RACEMES NOT SETTING PER NOT MATURE RACEMES RACEMES FLOWERING PODS /BRANCH /BRANCH BRANCH 12 9 13 16 13 8 11 77 20 0 0 0 62 38 50 84 10 97 22 60 0 45 45 0 25 69 28 50 99 98 60 86 0 38 96 74 100 100 100 100 25 96 12 100 100 98 100 100 0? 98 100 nc - data not collected 1Minumum estimate since more than 1 pod is set per raceme (mean= 2.5 pods/spike). These values were calculated based on lpod/ spike. 0 0 t5+ I t3 I 0 ; i ~ ~ :s: I / I II /0/0 1.0 0 I 2 i i 0.5 01 0 0 0 0 0 0 0 0 1 2 3 t-F L 0 WE RING - I 4 5 6 7 t----PODS--~ Fig. 2-3. Parental investment in terms of biomass and water in various stages of flowering and fruiting in Prosopis velutina. Flowering stages: 1-very immature racemes; 2-immature racemes; 3-mature flowering racemes. Pod stages: 4-very immature pods plus raceme (based on a mean of five pods per raceme); 5-elongate pods with undeveloped seeds; 6-green mature pods; 7-dry mature pods. w ....... Table 2-3. spikes per tree 850 Reproductive costs in tree LMP01 at site 1 in 1983. mean flowers per raceme racemes water biomass 188.6+61.4SD 91.97 41.22 % increase in cost ----------------- cost (grams per tree) immature pods mature pods water biomass water biomass 141.3 62.9 1764.6 2710 54% 53% 1100% 4200% w N 33 0 1.6 4 0 2 3 4 5 6 7 WEEKS Fig. 2-4. Cost of pod production in terms of dark respiration and biomass of pods in Prosopis glandulosa. Biomass and respiration both change most rapidly during the first two weeks of pod development. Associated with these high and rapidly changing costs is a very high abortion of immature pods. No abortion occurs after these first two weeks in P. velutina, when costs decrease. (Data from Wilson et al. 1974). 34 begins (Fig. 2-4; Wilson et al. 1974). Thus, prior to the second or third week of pod development, very little parental investment in biomass and water has occurred and the cost of maintaining the immature pods was greater than maintenance costs of more mature pods. Variability in Reproductive Output The mean number of pods and viable seeds per tree that were produced by all populations varied significantly between years and between populations (Table 2-4). Two-way analysis of variance of these factors .by year and site, with tree size as a covariate, indicated that the mean total number of pods produced per tree was strongly influenced by size of the tree, by year and by site effects, and that there was a significant interaction between year and site (Table 2-5). While the total number of seeds produced per tree differed between sites, there was not an overall year effect, but again there was a strong year by site interaction. and year. In Table 2-6 the data are presented by site These data explain the strong year by site interaction mentioned above. Not all sites showed similar variation in pod and seed production between years. Some sites showed significant variation between years (sites 4,5,6) while others did not (sites 1,2,3). Much of the variation between and within sites was explained by tree size (Fig. 2-5), with larger trees producing more pods and seeds and thus sites with older, larger trees produced more Table 2-4. Pod and seed production and abortion in P. velutina. Data are means+standard errors for six populations averaged over all all three years and for the average of all -six populations for each year of the study. The same letter after a value indicates a lack of significant difference within a column. SITE MEAN GOOD SEEDS PER MEAN PODS PER TREE 1765.:!:_300b M3 54.1+9.2b TREE M3 % OVULES # OVULES PER POD DEVELOP~lENT COMPLETING DEVELOPMENT DEVELOPING INTO GOOD SEEDS STARTING 12715.:!:_4206a 308.6.:!:_56.2a 14.9+0.45a 66.4+5.8b 76.6+3.5 49.7+5,2a 2 861+157a 28.5+7.2ab 8305.:!:_2106a 238.7.:!:_59.4a 13.6+0.62a 73.2+5.61ab 66.3+5.5 47.1+6,12a 3 241+62a 18.0.:!:_3.2a 4154.:!:_1053a 189.8.:!:_40,6a 13.6+0.74a 83,4+3.2a 89.8+2.3 67.1.:!:_3.6b 4 318+65a 23.9+5.2a 5503.:!:_1358a 462.9.:!:_114.6a 17.1+0.52b 83.7+4.0a 81.0+4.8 49.9+5,8a 609+144a 44.6+9.3ab 8596+2006a 520.2+115.2a 14.3.:!:_0.62a 89.1+2.1a 82.8+3.5 69.1+3.9b 2773+699b 32.0+7.2ab 47267+12374b 411.2.:!:_94.4a 15.5+0.34ab 90.2+1.7a 90.3+1.5 79.3+2.3b 1981 1620+410a 34.2+6.8a - 310+67.2 12.6.:!:_0.46a 79.6+2.4a 74.3+1.4a 60.1+3.4a 1982 1639+31la 50.0+7.1b 17776+5806 16837+5411 333+51.5 16.1+0.30b 62.8+4.5b 81. 9.:!:_1.4b 48.4.:!:_4.5b 1983 545+781b 27.2+4.4ab 10502+1491 409+65.7 15.1.:!:_0.34c 91. 5.:!:_1. 3c 82. 7+0. 7b 71.9.:!:_2.3c 6 YEAR w tTl 36 Table 2-5. Two-way analysis of variance of (A) the total number of pods per tree and (B) the total number of good (apparently viable) seeds per tree by year and by site, with tree size (foliage volume) as a covariate. All factors were significant for total pods, but total seeds were related mainly to tree size and population. The year by site interaction in both cases was a result of the high level of asynchrony between populations in space and over time. A. TOTAL PODS PER TREE Sum of Squares Covariate Size 16483 1 16483 72.5 0.000 Between Treatments 10635 7 1519 6.7 0.000 3960 6566 4848 2 5 9 1980 1313 539 8.7 0.000 5.8 0.000 2.4 0.017 Error 25223 111 227 Total 57190 128 447 Year Site Interaction B. Degrees of Freedom p Source of Variation Mean Square F TOTAL GOOD SEEDS PER TREE Sum of Squares Degrees of Freedom Covariate Size 180029 1 180029 54.7 0.000 Between Treatments 51231 7 7319 2.2 0.039 855 50269 103619 2 5 8 428 10054 12952 0.1 0.878 3.1 0.013 3.9 0.000 Error 305893 93 3289 Total 640772 109 5879 Year Site Interaction fv1ean Square F p Source of Variation Table 2-6. YEAR Pod and seed data for each site by year ( mean~ SE) for 6 populations of Prosopis velutina. MEAN PODS PER TREE MEAN GOOD SEEDS PER M3 TREE M3 I OVULES PER POD SITE 1981 2200+760 51.9~12.9 22343~12393 1962 2035+363 75.6~22.8 3769~1005 1983 1082+238 36.6+9.8 12095+2712 18.0~4.5 5611+2643 138+53.9 43.6~19.6 7082+3419 268+134.3 14854+5260 370+111.3 :t OVULES STARTING DEVELOPMENT COMPLETING DEVELOPI·IENT DEVELOPING INTO GOOD SEEDS 457.6~102.4 13.7+0.9 83.0~3.0 80.2~4.8 66.4+4.6 99.2~32.3* 16.2+0.7 13.7~3.3* 66.5+9.5 10.6+3.0* 14.9+0.6 85.2+2.0 79.7+3.6 68.3+4.0 12.3+0.7 72.4+6.0 61.5+10.5 47.3+9.8 15.1+0.9 49.1+13.7 64.1+8.0 33.8+10.2 14.0+1.8 83.9+2.5 79.0+5.2 66.6+6.1 10.8~1.1* 65.4~6.1a 92.3~4.8 60.8+7.3 363.5~104 •• SITE 2 1981 704+267 1982 1032~230 1983 84 7+335 23.8~7.5 SITE 3 1981 88+30 1982 394+113 l5.8~3.4 5820+1018 279+59.2 15.9~0.8 72.4~4.7ab 92.0+2.7 67.0+5.8 1983 212+98.8 18.3~5.0 4495+2085 200+58.6 14.6~0.8 85.7~2.3b 85.4~3.7 73.6+5.0 1982 710~111* 55.7~6.3* 6078~1838 17.1~0.7 57.3~6.3 77.8~6.3 45.8+7:2 1983 111~52.2 0.3~0.2* (4064~1284) 17.2.:~0.2 68.4~10.8 89.1~4.2 60.0!_8.4 1984 212+97.2 15.7~6.1* 11.4+0.9* 81.3+4.6 69.2+6.8* 56.0+6.0a 607.6+218.8 .16.1+0.7 - 76.7+4.5 92.7~2.5 71. 4+5. 5ab 8590+2948ab 718.8+171.2 15.3+0.8 88.8+3.7 86.6+4.8 77.6+6.3b 4.3~0.4* 699+283* 20.3+4.2* SITE 4 SITE 1981 219+92 8.5~3.8* 1457+766 - 57.9+34.3* - 1982 1374+316* 55.1~21.4 1983 335+138 57.6+12.0 1981 5149+1168 64.2~19.3* 60856.!_14042 775~245 15.6~0.4 83.9+3.4 90.6+1.6 76.0+3.5 1982 3891+1543 24.2~7.5 62538~25347 341~113 15.8+0.5 87.6+2.5 92.1+1.9 81.0+3.7 1983 996+348* 20.9~9.6 17847+4869 262+140 15.1+0.7 88.3+3.3 89.9+3.4 79.3+4.3 14553+3763b - - SITE 6 *a6~- Different letters or a * indicate a significant differenc~ between years within one site (Scheffe's multiple range test P=0.05). 1- Numbers in parentheses are based on only the trees that produced pods within .that site in that year. w ....... Y=16.7 X+ 317.6 0 R2 = 0.515 0 0 3000 0 2000 0 (./) 0 0 £l.. 0 z 0 I 0 0 0 0 1000.l 0 0 oA 6 0 6 ~ 0 D. Q 6 606 ~Q 6 40 80 TREE SIZE 120 160 (m3l Fig. 2-5. Relationship of pod production wi~h tree size (foliage volume) in P. velutina. The symbols represent the six different populations. Site 1 - 0 ; Site 2 - D ; Site 3 - ~ ; Site 4 - 0; Site 5 - 0 ; Site 6 - 0 . Over 50% of the variation in pod production is explained by tree size. w co 39 pods and seeds. There was also an apparent alternate year pod production pattern (Fig. 2-6). Trees that produced few pods in 1981 produced a greater number of pods in 1982 and trees that produced high numbers of pods in 1982 similarly produced few to no pods in 1983. A comparison of production by trees in 1981 and 1983 comes closer to a one to one correspondence between how many pods each tree produced in 1981 and 1983. Thus trees that produced high numbers of pods in a good year (1982) produced few or no pods in the prior (1981) and succeeding (1983) years, while pod production in both poor years was equivalent. Tree size and alternate year production by individual trees and populations explains 36 to 58% of the variation in seed and pod production in Prosopis velutina. Much of the remaining variation was due to between-tree variation within a site. Synchrony of flower, fruit and seed production was relatively high within each site, but a few trees at each site either produced every year or were simply out of synchrony with the majority of the population and produced large seed crops in "off" years. All trees at site 1 (McGuireville) produced pods consistently every year (although seed abortion rates still cycled on an alternate year basis). At site 3 (West Clear Creek) trees 1 and 2 produced heavily in 1980 and 1983 while the rest of the population had high pod production in 1982 and produced no pods in 1983. 40 r :.462 p :.005 N=30 5600 4200 ~ 2800 1400 ...... 0 1982 r:.404 p:,OI 2 N=31 5600 4200 ~ 2800 1400 0 . 1983 r ~.43 7 p =.001 N =51 4200 2800 N 00 2:' 1400 • .. 0 0 1400 2800 4200 5600 1983 Fig, 2-6. Pod product1on in Prosop1s velutina over three years. These year aga1nst year plots demonstrate the alternate year pod production pattern for ind1vidual trees. r~ote that in 1981 and 1983, the relationship 1s close to 1:1 and that trees that produced no pods in one year exhlbited a h1gh pod product1on the following and/or prev1ous year. 41 The above data indicate some proximal causes for intersite and interyear variation in fruit and seed production, but it would be more meaningful to seek the ultimate causes for these reproductive patterns. These ultimate causes appear to be linked to the resource relations of each individual tree, since other factors such as rainfall and tree density (i.e., climatic and population parameters) were poorly related to seed production. Although tree size was significantly related to pod and seed production (Fig. 2-5), the relationship was not direct as might be expected. Instead, as tree size increased, fewer pods were produced per unit volume of tree, so that smaller trees were actually more productive per unit volume (Fig. 2-7). This indicates a cost involved in the maintenance of larger tree biomass and a tradeoff in maintenance and reproductive costs. There was also a distinct tradeoff between growth and reproduction, with trees that produced pods rarely producing any new growth after leafing. Trees that did not produce pods would often have branch growth of up to 60 ern. Finally, these trees showed a distinct inability to mature either all ovules (assuming fertilization was not limiting - see discussion) or even to mature all seeds that began development. There was a consistent relationship between reproductive investment and reproductive gain (Fig. 2-8) for most trees. However, those trees which produced pods every year, such as those at site 1 in 1982, showed a • 160 Y= 0.62 X+ 44.42 p <0.05 r =0.2 7 1'0 E 120 0:: w • I a_ l/) 0 0 a_ 80 I z <( w ~ 40 • • ,~ I Ot_ 0 . • • • • • • • •• •• • • •• • • •• • •• • • • • • • • • • • 60 • •• 120 180 240 TREE SIZE (m3) Fig. 2-7. The number of pods produced per unit volume of tree foliage (m3) as a function of tree size. As tree size increased there was a significant decrease in the number of pods produced per unit volume of tree foliage. .j:::> N ~OBSERVED:• · • • 1200 r2=.872 • • r0 E '800 (./) 0 w w (./) 400 I I !:J' .,. • • SITE 1: 82:o r2=.875 • ' 0 • 0 0 • 100 PODS 1m3 0 200 Fig. 2-8. Reproductive gain (number of good seeds produced) as a function of reproductive investment (pod production) in P. velutina. Most of the outliers (open circles) were trees at site 1 in 1982,-where trees produced many pods but very few seeds matured successfully (these points were excluded from the observed regression). All points lie below the maximal reproduction expected if all seeds developed successfully. Regression equations: Exp.-Y=16.8X; Obs.-Y=10.1X; Site 1 1982 - Y=1.22X. +::> w 44 much lower benefit in seeds produced for a similar investment in pod material compared to 1981 and 1983. This drop in proportion of good seeds produced did not occur in the other populations where pod production varied more between years (Fig. 2-8). The proportion of ovules that began development into seeds was ususally lower and more variable (Tables 2-4,2-6) than was the proportion of these ovules that completed development into viable seeds. This seems to indicate that once a commitment was made by the parent tree to develop a seed, that the seed had a high probability of successful development. Variation in the proportion of seeds that failed to develop once development was initiated was most likely due to herbivore damage and probably was less a result of active abortion by the parent plant (see chapter 3). DISCUSSION This study indicates three aspects of flowering in Prosopis velutina that may be of evolutionary and adaptive significance. First, flowering phenology was more variable than all other reproductive parameters. Flowers were produced by almost every tree in every year but there was a wide fluctuation within and between populations as to the number of inflorescences initiated and the timing and length of the major flowering period. Flowering was typically initiated in association with spring budbreak and growth - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - 45 after the soil temperature exceeded 18°C (Meyer et al. 1973, Simpson et al. 1977). This temperature was reached in mid-April in 1981, but usually does not occur before mid-May. As a result most all populations flowered earlier in 1981 than in other years. Site 5 (Copper Canyon) did not follow this pattern but showed a high consistency of initiation of flowering in the last half of May over all three years. Site 6 (Cottonwood) produced pods much later in 1981 than all other sites. Flowering typically lasted for about 30 days but in several cases extended over a 45 day period. Reproductive synchrony is the norm for mass-flowering, obligately-outcrossing, insect-pollinated trees and shrubs. Flowering out of sequence with the rest of the population or populations lowers pollinator attraction and constancy, increases flower and seed predation and increases intraplant resource competition (Augsperger 1981, Doust and Eaton 1982). Thus in species like Prosopis velutina, reproductive consistency should be under intense selection. This raises the question as to why synchrony of flowering was so sloppy in this system. Synchrony is much tighter in other species of mesquite which live in much harsher environments (Simpson et al. 1977). Variability in flowering needs to be examined more rigorously to further address this question. Secondly, the trees in these populations consistently produced many more flowers than they were physiologically or structurally able to mature into fruits and seeds. Such 46 apparently wasteful flower production is common in the legume subfamily Mimosoideae (Solbrig and Cantina 1975) and in many other plant groups (Augsberger 1981). The major hypotheses dealing with this phenomenon have to do with the attraction of insect pollinators to ensure adequate outcrossing (Solbrig and Cantina 1975, Willson 1983, Willson et al. 1979), thereby increasing associated seed production. However, such large floral displays may also function to increase male reproductive success (Sutherland and Delph 1984). Since pollinators are probably not limiting in mesquite and pollen viability is high (75% in Prosopis farcata in Israel - Dafni and Negbi 1980), it is likely that such large and varied amoun·ts of pollen might increase male fitness. Alternately, since a large proportion of flowers (or racemes) never produce fruit, the plant may select for certain pollen-ovule combinations (Willson 1983). Thirdly, there must be a considerable cost involved in flower production. In all populations a large number of racemes were dropped by trees even before flowering. Although herbivores may account for some of this abortion, herbivore damage was often absent. This occured more commonly in years following a large seed crop the previous year. Pre-flowering raceme drop was most prominent in dry, hot spring weather when rainfall was scarce and nitrogen is most limiting (Glendening and Paulsen 1955, Shearer et al. 1983). Thus, the tree must reach some point at which costs exceed available resources. At this point, pre-flowering 47 racemes, which are relatively cheap (see Table 2-3, Fig. 2-3), are aborted before parental investment costs can accumulate. Sometimes a successful reproductive bout is then attempted later when nutrient reserves have increased and water is more plentiful. Supra-annual fruiting patterns, such as those seen in mesquite in this study, are thought to be a response to either insect seed predators (Silvertown 1980, Janzen 1969, Johnson and Slobodchikoff 1979) or to the necessary accumulation of resources required to produce an optimal seed crop or both (Stephenson 1981, 1984). In the first case, there is a high level of synchrony of seed production within a population (Sork 1983, Silvertown 1980, DeStephen 1982). The lack of significant differences for many of the parameters in Tables 2-4 and 2-6 are an indication of the extreme lack of synchrony within these mesquite populations. Trees that produced out of synchrony produced just as many pods, and viable seeds, while the synchronous portion of the population produced no fruit at all. This asynchrony resulted in_ high levels of inter- and intra-population variablity in fruit and seed production and in fruit and seed abortion. This seems to point to a relative unimportance of seed predators as selective agents in mesquite reproductive. strategies (see chapter 3). At the same time, it supports the alternative energy limitation hypothesis, which proposes that each plant must accumulate a given amount of resources to reproduce. 48 Many potential selective factors may also act against synchrony. According to Silvertown (1980), synchrony is not to be expected in a species with animal dispersed, fleshy fruits. Mesquite produces a highly edible nutritious pod with seeds that are dispersed (and seed germination improved) mainly by passage through a vertebrate digestive tract (endochory) (Glendening and Paulsen 1955, Janzen and Martin 1981, Felker et al. 1984). Thus any selection for synchrony might be counterbalanced by selection for the maintenance of a population of dispersal agents. production of pods, which con~ain The no or few viable seeds, by the mesquite trees in this study (especially site 1 in 1982) might circumvent this problem by providing maintenance of dispersal agents at a much lower cost (no seed production)· and yet still allow a relatively high level of synchrony in seed production in alternate years. This variation in itself might also serve to decrease the effects of seed predators in off-years, by increasing the uncertainty of finding fruits in any given population or on any given tree, or even of finding a suitable host seed within any given pod, where only 1 or 2 seeds out of 15 may be suitable hosts. Some of these alternative explanations for variability in seed production are discussed in chapter 3. A large number of plants are able to match fruit and seed number with available resources over an extremely wide range of environmental conditions. Thus the production of flowers every year and the subsequent abortion of flower 49 buds, flowers, racemes, fruits, and ovules and seeds might represent a bet-hedging strategy for seed production in a variable and highly unpredictable desert environment (Stephenson 1981, Stearns 1976, Wilbur et al. 1974). Evidence for Environmental Limitation in Mesquite Evidence points to both water and nutrient stress in several species of mesquite. In this study there was an obvious tradeoff between growth and reproduction. Trees that produced large numbers of fruits did not grow significantly. Turner et al. (1963) also found that radial growth was depressed during fruiting. Seed production per unit volume of tree also decreased significantly as size of the tree increased. Mature mesquite trees suffer heavy mortality in periods of drought (Carter 1964, Judd et al. 1971). Thus as tree size increases, the cost of maintenance apparently decreases the amount of energy that can be allocated to reproduction. Even the cost of maintenance can be excessively high under extended stress conditions, resulting in tree death. Water stress, which is the major limiting factor in a desert environment, has been well documented in several Prosopis species. In southern Arizona, extensive mesquite stands cause a 30mm diurnal variation in the water table (Tremble, 1977). Severe water stress is common from May to August in Prosopis glandulosa in the Sonoran Desert in southern California, even though soil water content at a 50 depth of 5.5 m remains constant (Nilsen et al. 1981, 1983, 1984). The high levels of evapotranspiration required for maintenance may cause water to be limiting for other plant functions such as flowering and pod production (Meyer et al. 1973, Strain 1970). Even the extensive lateral and deep tap root systems of Prosopis which allow use of underground water (Phillips 1963) may not allow a phreatophytic plant like mesquite to be free of water stress in these harsh desert environments. They must use water as it becomes available and then go into a stage of limited metabolic activity until more water becomes available (Felker et al. 1980, 1984). Nutrients are also limiting in many semi-arid, overgrazed ecosystems common to the desert Southwest (Felker et al. 1980). Next to water, nitrogen is probably the next most important limiting factor in desert ecosystems. Prosopis species are to some extent free from nitrogen limitation by their ability to form nodules with nitrogen fixing bacteria (Felker and Clark 1980, Eskew and Ting 1978). Thus nitrogen under mesquite trees is often much higher than in areas surrounding mesquite populations (Tiedemann and Klemmedson 1973, Virginia et al. 1982). Much of this litter and soil nitrogen is unavailable to the trees because of the low leaching and mineralization rate due to low rainfall of desert areas (Virginia and Jarrell 1983}. Studies of the use of nitrogen from soil ·and fixation (atmospheric nitrogen} indicate a high use of soil nitrogen 51 (not stored or fixed) for spring flower and leaf production, while the nitrogen used for pod and seed production is mostly fixed (Shearer et al. 1983). Therefore Prosopis species in the desert Southwest may be nitrogen limited in the spring when rainfall is low and nitrogen is taken mainly from nitrogen leached to the roots by winter and spring rainfall, before soil temperatures increase enough to allow fixation by the associated symbiotic bacteria. In years with extremely low spring rainfall, water and nitrogen limitation may act together to limit both growth and reproduction in mesquite. Photosynthetically produced carbohydrates may also significantly limit growth and reproduction in mesquite. Photosynthesis by pods and leaves of Prosopis glandulosa in Texas only produces one-third of the necessary photosynthate necessary for the growth and energy demands of the developing fruits alone. Trees with many developing pods show a rapid depletion of available stored root carbohydrates (Wilson et al. 1974). Further studies have shown that bud break, flowering and seed formation are all strongly dependent on stored carbohydrates (Wilson et al. 1975, Fick and Sosebee 1981). All these studies strongly support the hypothesis that flower, pod, and seed production is an expensive energy and nutrient drain on the individual tree and that these factors play an important role in both the variability in fruit and seed production in t· velutina and in the extensive and 52 variable abortion of flower buds, inflorescences, fruits, and seeds as well as in the imperfect alternate year seed production patterns noted in this study. The high variability which was prominent fn the mesquite populations in this study indicates that the highly uncertain environment may have selected for a bet-hedging strategy in these plants. The cost of flower production was relatively cheap, and so a strategy of producing flowers every year, and then only maturing as many fruits and seeds as environmental and resource limitations will allow, could be optimal. If these limitations are extreme then the tree might not be able to reproduce at all. Since environmental predictability is low in desert ecosystems this might be a safer strategy than a strictly synchronous alternate year production strategy. Conversely, such a strong environmental-resource role in determining reproductive stategies in Prosopis velutina would tend to minimize the role of seed predators as agents of selection on reproductive processes, and also indicate a relatively important role for dispersal agents as a selective force on mesquite reproductive strategies. 53 LITERATURE CITED Augspurger, C.K. 1981. Reproductive synchrony of a tropical shrub: Experimental studies on effects of pollinators and seed predators on Hybanthus prunifolius (Violaceae}. Ecology 62:775-788. Bell, E.A. 1978. Toxins in seeds. Harborne (ed). pp. 143-161, In: J.B. Biochemical aspects of plant and animal coevolution. Academic Press, New York. Carter, M.G. 1964. Effects of drouth on mesquite. J. Range Manage. 17:275-276. Dafni, A. and M. Negbi. 1978. Variability in Prosopis farcta in Israel: seed germination as affected by temperature and salinity. Isr. J. Bot. 27:147-154. Dafni, A. and M. Negbi. 1980. Variability in Prosopis farcta in Israel: fertility and seed production in populations from different habitats. Acta Oecol. Oecol. Plant. 1:335-344. DeStephen, D. 1982. Seed production and seed mortality in a temperate forest shrub (witch hazel, Hamamelis virginiana). J. Ecol. 70:437-443. Doust, J.L. and B.W. Eaton. 1982. Demographic aspects of flower and fruit production in bean plants, Phaseolus vulgaris L. Amer. J. Bot. 69:1156-1164. 54 Eskew, D.L. and I.P. Ting. 1978. Nitrogen fixation by legumes and blue-green algal-lichen crusts in a Colorado desert environment. Amer. J. Bot. 65:850-856. Felker, P.H. 1979. Mesquite: an all-purpose Leguminous arid land tree. p. 89-132, In: G. A. Ritchie (ed). New Agricultural Crops, Westview Press, Boulder, Colorado. Felker, P. and P.R. Clark. 1980. Nitrogen fixation (acetylene reduction) and cross inoculation in 12 Prosopis (mesquite) species. Plant and Soil 57:177-186. Felker, P., P.R. Clark, J. Osborn, and G.H. Cannell. 1980. Nitrogen cycling-water use efficiency interactions in semi-arid ecosystems in relation to management of tree legumes (Prosopis). Unpub. mss. presented at International Symposium on browse in Africa, International Livestock Center for Africa, Addis Abba, Ethiopia, April 1980. Felker, P., P.R. Clark, J.F. Osborn, and G.H. Cannell. 1984. Prosopis pod production-composition of North American, South American, Hawaiian, and African germ plasm in young plantations. Econ. Bot. 38:36-51. 55 Fick, W.H. and R.E. Sosebee. 1981. Translocation and storage of 14C-labeled total nonstructural carbohydrates in honey mesquite. J. Range Manage. 34:205-208. Glendening, G.E. and H.A. Paulsen. 1955. Reproduction and establishment of velvet mesquite, as related to invasion of semidesert grasslands. U.S. Dept. Agric. Tech. 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Teran. 1977. Prosopis fruits as a resource for invertebrates. pp. 108-122, In: B.B. Simpson (ed). Mesquite, its biology in two desert scrub ecosystems. Dowden, Hutchinson and Ross, Stroudsburg, PA. Lechowicz, M.J. 1984. Why do temperate deciduous trees leaf out at different times? Adaptation and ecology of forest communities. Am. Nat. 124:821-842. Lowe, C.H. 1964. Arizona•s Natural Environment; landscapes and habitats. Univ. Arizona Press, Tucson, 136 pp. McMillan, C. and J.T. Peacock. 1964. Bud-bursting in diverse populations of mesquite (Prosopis:Leguminosae) under uniform conditions. Southwestern Nat. 9:181-188. Meyer, R.E. and R.W. Bovey. 1982. Establishment of honey mesquite and huisache on a native pasture. J. Range Manage. 35:548-550. Meyer, R.E., R.H. Haas, and C.W. Wendt. 1973. lnteraction of environmental variables on growth and development of honey mesquite Bot. Gaz. 134:173-178. 57 Meyer, R.E., H.L. Morton, R.H. Haas, E.D. Robison, and T.E. Riley. 1971. Morphology and anatomy of honey mesquite. U.S. Dept. Agric. Tech. Bull. 1423:1-186. Nilsen, E.T., P.W. Rundel and M.R. Sharifi. 1981. Summer water relations of the desert phreatophyte Prosopis glandulosa in the Sonoran Desert of southern California. Oecologia 50:271-276. Nilsen, E.T., M.R. Sharifi, and P.W. Rundel. 1984. Comparative water relations of phreatophytes in the Sonoran Desert of California. Ecology 65:767-778. Nilsen, E.T., M.R. Sharifi, P.W. Rundel, W.M. Jarrell, and R.A. Virginia. 1983. Diurnal and seasonal water re~ations of the desert phreatophyte, Prosopis g~andulosa (honey mesquite) in the Sonoran Desert of California. Ecology 64:1381-1393. Paige, K.N. and T.G. Whitham. 1985. Individual and population shifts in flower color by scarlet gilia: a mechanism for pollinator tracking. Science 227:315-317. Phillips, W.S. 1963. Depth of roots in soil. Ecology 44:424. Pyke, G.H. 1978. Optimal foraging in bumble bees and coevolution with their plants. Oecologia 36:281-291. 58 Schaffer, W.M. and M. Gadgil. 1975. Selection for optimal life histories in plants. pp. 142-157, In: M.L. Cody and J.M. Diamond (eds. ). Ecology and evolution of communities. Belknap Press, Cambridge, Massachusetts. Shearer, G., D.H. Kohl, R.A. Virginia, B.A. Bryan, J.L.Steeters, E.T. Nilsen, M.R. Sharifi and P.W. Rundel. 1983. Estimates of N -fixation from variation in the natural 2 abundance of lSN in Sonoran Desert ecosystems. Oecologia 56:365-373. Silvertown, J.W. 1980. The evolutionary ecology of mast seeding in trees. Biol. J. Linn. Soc. 14:235-250. Simon, J.-P. 1979. Cqmparative serology of a disjunct species group: complex. The Prosopis juliflora - Prosopis chilensis Aliso 9:483-497. Simpson, B.B. 1977a. Breeding systems of dominant perennial plants in two disjunct warm desert ecosystems. Oecologia 27:203-236. Simpson, B.B. (ed). 1977b. Mesquite, its biology in two desert scrub ecosystems. Dowden, Hutchinson and Ross, Stroudsburg, PA. Simpson, B.B., J.L. Neff, and A.R. Moldenke. 1977. Prosopis flowers as a resource. pp. 84-107, In: B.B. Simpson (ed). Mesquite, its biology in two desert scrub ecosystems. Dowden, Hutchinson and Ross, Stroudsburg, PA. 59 Smith, C.C. 1975. The coevolution of plants and seed predators. (eds). pp. 53-77, In: L.E. Gilbert and P.H. Raven Coevolution of Animals and Plants. Univ. Texas Press, Austin. Smith, L.L. and D.N. Ueckert. 1974. Influence of insects on mesquite production. J. Range Manage. 27:61-65. Solbrig, O.T. and K.S. Bawa. 1975. Isozyme variation in Prosopis (Leguminosae). J. Arn. Arb. Harvard Univ. 56:398-412. Solbrig, O.T. and P.O. Cantino. 1975. Reproductive adaptations in Prosopis (Leguminosae, Mimosoideae). J. Arn. Arb. Harvard Univ. 56:185-210. Sork, V.L. 1983. Mast fruiting in hickories and availability of nuts. Am. Midl. Nat. 109:81-88. Stearns, S.C. 1976. Life-history tactics: a review of the ideas. Quart. Rev. Biol. 51:3-47. Stephenson, A.G. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annu. Rev. Ecol. Syst. 12:253-279. Stephenson, A.G. 1984. The cost of over-initiating fruit. Am. Midl. Nat. 112:379-386. 60 Strain, B.R. 1970. Field measurements of tissue water potential and carbon dioxide exchange in the desert shrubs Prosopis julifera and Larrea divaricata. Photosynthetica 4:118-122. Sutherland, S. and L.F. Delph. 1984. On the importance of male fitness in plants: patterns of fruit-set. Ecology 65:1093-1104. Tiedemann, A.R. and J.O. Klemmedson. 1973. Nutrient availability in desert grassland soils under mesquite (Prosopis juliflora) trees and adjacent areas. Soil Sci. Soc. Amer. Proc. 37:107-111. Tromble, J.M. 1977. Water requirements for mesquite (Prospis juliflora). J. Hydrology 34:171-179. Tschirley, F.H. and S.C. Martin. 1960. Germination and longevity of velvet mesquite seed in soil. J. Range Manage. 13:94-97. Turner, R.M. 1963. Growth in four species of Sonoran Desert trees. Ecology 44:760-675. Virginia, R.A. and W.M. Jarrell. 1983. Soil properties in a mesquite dominated Sonoran Desert ecosystem. Soil Sci. Soc. Am. J. 47:138-144. 61 Virginia, R.A., W.M. Jarrell, and E. Franco-Vizcaino. 198l. Direct measurement of denitrification in a Prosopis (mesquite) dominated Sonoran Desert ecosystem. Oecologia 53:120-122. Werker, E., A. Dafni, and M. Negbi. 1973. Variability in Prosopis farcta in Israel: anatomical features of the seed. Bot. J. Linn. Soc. 66:223-232. Wilbur, H.M., D.W. Tinkle and J.P. Collins. 1974. Environmental certainty, trophic level, and resource availability in life history evolution. Am. Nat. 108:805-817. Willson, M.F. 1983. Plant reproductive ecology. John Wiley and Sons, New York, 282pp. Willson, M.F., L.J. Miller and B.J. Rathcke. 1979. Floral display in Phlox and Geranium: adaptive aspects. Evolution 33:52-63. Wilson, R.T., B.E. Dahl and D.R. Krieg. 1974. A physiological study of developing pods and leaves of honey mesquite. J. Range Manage. 27:202-203. Wilson, R.T., B.E. Dahl, and D.R. Krieg. 1975. Carbohydrate concentrations in honey mesquite roots in relation to phenological development and reproductive condition. J. Range Manage. 28:286-288. CHAPTER 3 Reproductive Strategies in Prosopis velutina (Leguminosae) and Their Effect on Seed Predation 62 by Bruchid Beetles 63 INTRODUCTION Mortality, of flowers, fruits and seeds, caused by animals has long been thought to play a very important role in the evolution of reproductive strategies in plants. Inflorescence and flower structure, numbers and phenology are strongly influenced by animals ~hat act as either pollinators or as predators of pollen, nectar, and flower-ovule tissues (Willson 1983, Heithaus et al. 1982, Willson and Price 1977, Willson and Rathcke 1974). Fruit herbivores and seed predators have also been hypothesized to be important selective agents affecting plant population parameters such as spacing, seedling recruitment, and plant diversity (Louda 1982, Clark and Clark 1984, Risch 1977, Vandermeer 1974, Wilson and Janzen 1972, Janzen 1970, 1971), as well as the timing and extent of seed production (Sork 1983, Silvertown 1980, Janzen 1976, Green and Palmblad 1975). These predators supposedly also influence the allocation of resources to reproduction by selecting for chemical, morphological or numerical defenses of the host plants (Bradford and Smith 1977, Hare 1980, Janzen 1969, 1983, Mitchell 1977, Moore 1978b) or for mechanisms of dispersal to escape predation (Janzen 1983, Solbrig and Cantino 1975). Plants thus possess a large variety of population and individual traits that seem to decrease the effects of predators upon their reproductive output. 64 The relative value of insect seed predators as selective agents on plants and their reproductive strategies has rarely been examined in context with other, perhaps more -important, selective forces acting on plant reproductive output. These other factors may either constrain, oppose or outweigh evolutionary responses of plants to selection by seed predators. Such factors may include growth rates, seed germination, seedling survival, physiological responses to environmental variables, and nutrient or resource limitation. All of these may strongly influence reproductive strategies. Willson (1983) and Heithaus et al. (1982) attempt to place all of these diverse selective forces into perspective and discuss alternative ways of dealing with seed production strategies. Heithaus et al. (1982) examined multiple mortality factors affecting seed production in Bauhinia ungulata (Leguminosae) in one of the few comprehensive studies. They found that seed predators were fourth out of seven factors in their importance to seed and fruit mortality. Further comprehensive studies are required to provide more evidence for the selective importance of seed predators in the evolution of plant reproductive strategies. The Bruchidae (Coleoptera) have been repeatedly assumed to be or have been in the past a potent selective force on their host plants. These beetles are obligate seed predators and are highly host specific, mainly attacking seeds of plants in the family Leguminosae (Johnson 1981a, 65 Janzen 1980). Intense coevolutionary interactions have been hypothesized to have occurred as a result of this highly specialized seed predation (Center and Johnson 1974, Janzen 1969, Johnson and Slobodchikoff 1979, Johnson 1981b, Johnson and Kistler 1985, Kistler 1982). This study addresses two questions dealing with the relative importance of seed predation by a guild of four desert bruchids on seeds of velvet mesquite (Prosopis velutina Wooten), a phreatophytic desert tree or shrub. The primary question was whether seed predation by these bruchids was a significant factor, when examined both by itself and in relation with other potential selective forces acting on the reproductive output of mesquite. A secondary question was whether reproductive strategies of mesquite have a negative impact upon bruchid or other seed predators that might limit the bruchid populations and their evolution as significant seed predators. METHODS The study was conducted in the Verde Valley of central Arizona, USA, from April, 1981, to December, 1983. The Verde Valley is an area of upper Sonoran Desert scrub and desert grassland (Lowe 1964). A more detailed description of the area can be found in chapter 2. Prosopis velutina ranges in size from a small shrub to a moderate sized tree and grows mainly along dry washes, 66 adjacent to riparian areas, or in flood plains, where water is relatively abundant. Mesquite is a phreatophyte with root systems often extending 80 meters to reach abundant sources of ground water. As a result it can be highly affected by periods of low rainfall (Carter 1964, Nilsen et al. 1983, Solbrig and Cantino 1975). Flowering and fruit production generally occur in the spring, soon after air temperatures exceed 67 0 F (Meyer et al. 1971). self-incompatible (Simpson et al. 1977). Flowers are Of the approximately 150 - 200 flowers that occur on each inflorescence (raceme), fewer than seven will set fruit and less than half of these will survive to produce mature seeds •. Of the several thousand racemes on any one tree, a large proportion fail to produce any fruits. The flowers are insect pollinated and attract pollinators to the very rich source of pollen and nectar. Thus pollination is not thought to limit fruit set (Simpson et al. 1977). The fruit is an indehiscent legume pod with 10-25 ovules per pod. These pods contain large amounts of sucrose (13-36%) and thus attract numerous vertebrate dispersal agents which consume the pods and pass the seeds through the gut, providing both dispers~l away from the parent tree and increased germination success (Felker 1979, Kingsolver et al. 1977). Flowering and fruit set were monitored during 1983. Each population was visited every two weeks throughout the season. The number of racemes per tree was estimated by - 67 averaging the number on four branches and multiplying by the number of branches per tree. In this manner the number of racemes produced, the number that eventually flowered (>50% flowering) and the number of pods produced per tree were recorded. Seed set and predation were monitored for three years (1981-1983). Thirty pods were collected at random from each tree (5-10 trees/site), at each site, every 7-14 days after the seeds began to mature in the pods. Each 30 pod sample was placed into a one quart mason jar with a paper towel top, impregnated with 1% Kelthane to prevent infestation by pyemotid mites. Emergence of all seed insects was monitored weekly for 50 days after collection. All samples collected from each tree in one year were grouped together to determine a mean predation rate for each tree in each year. This mean value should give the most accurate estimate of the number of seeds that were destroyed ·by the seed predators, over the entire season, since predation rate increased as the resource pool was decreased by pod dispersal. One sample collected from each tree just prior to or after pod fall was examined in detail after the 50-day emergence period. All 30 pods of each sample were visually examined and the number of seeds destroyed by Bruchidae, Lepidoptera, and miscellaneous herbivores was recorded. The number of ovules per pod was counted, and each ovule was classified (based mainly on pod thickness) as showing either 68 no development, some development or completed development into a mature seed. A subsample of pods from each site was dissected and again each seed-ovule was classified into one of these three classes. Although there was good agreement between the visually examined and the dissected samples the dissection data provided a more accurate estimate of the stage to which an ovule had developed or the cause of death. Through a field bioassay, I examined whether there was evidence of selection by seed predators for synchrony of pod production within a population. Site 5 (Copper Canyon) consisted of two discrete populations with one-half of the entire population producing pods each year. In 1983, the southern population failed to produce any pods (<100 pods /site), while over 90% of the northern population which is directly adjacent, produced numerous pods per tree. To examine what levels of seed predation might occur in the seeds of a tree that produced pods out of synchrony with the rest of the population, five hardware cloth cages (.635 em mesh) each containing 15 pods from the 1982 crop of tree #4 at site 5, were hung within the canopy of tree #4, a tree in the middle of the southern (no pod) population, in 1983. other pods were present within 1 km. No These cages were left in the tree for 30 days and were then collected and the seed predators reared as described above. 69 RESULTS Flower Production and Mortality Some trees failed to initiate flower poduction in some years, but, on the whole, the majority of trees did initiate production of inflorescences every year. Flowering usually occured in late April to May and was highly synchronous within a population of trees. There was, however, a very wide range of numbers of racemes produced by a tree. This number varied between years, even within the same tree. In 1983, the number of racemes per tree ranged from 80 to 4480 and the number per branch ranged from 10 to 150. Although the loss in·potential reproductive output, resulting from producing fewer than the maximum number of inflorescences possible every year, may be an important part of the plant•s reproductive strategy (via conservation of resources for subsequent reproduction), it was not quantified in this study. Once inflorescences had been initiated the chance of a given raceme actually producing fruits was less than 50%. The tree often aborted entire racemes even before the flowering buds had matured and in 1983 up to 100% of all pre-flowering racemes were aborted from trees at sites 4 and 5, although the (Table 3-1). ~ite means only ranged from 21.4 - 85.3% Some of this abortion may be due to herbivores, especially curculionid beetles, but a larger portion seems to be based on resource limitation in the Table 3-1. The number of inflorescences produced and setting fruit in six populations of Prosopis velutina in 1983. Values are means of the mean value for each tree. SITE DENSITY #/Ha X TREE SIZE (m3) MEAN NUMBER IMMATURE RACEMES/TREE MEAN NUMBER ·No. MATURE FLOWERING RACEMES SETTING RACEMES/TREE FRUIT % RACEMES LOST BEFORE FLOWERING % RACEMES % FLOWERING LOST BEFORE RACEMES LOST BEFORE SETTING FRUIT SETTING FRUIT 480 58.9 1742 1369 768 21.4% 55.9% 43.9% 2 64 37.2 2124 1126 633 47.0% 70.2% 43.8% 3 119 22.4 1741 1163 261 33.2% 85.0% 77.6% 4 337 13.6 464 146 2 68.5% 99.5% 98.6% 5 670 21.4 1918 282 13 85.3% 99.3% 95.4% 6 158 127.3 1974 503 no data 74.5% no data no data ......, 0 71 individual parent plant (chapter 2). Of those inflorescences that actually flowered, 44-99% failed to set any fruit. These values are minimum estimates, since each raceme produced on the average 1 •. 5 mature fruits and these values include both the number of racemes dropped without setting any fruit and the number of immature pods dropped during the first two weeks of fruit development, when fruit abortion occured (chapter 2). Non-predation Ovule and Immature Seed Mortality Only data from the pods actually dissected were used to obtain the estimates of ovule mortality. falls into two classes. A significant number of ovules failed to initiate development (95% CI: ovules). Such mortality 30.0-35.8% of all One-way analysis of variance indicates that this factor varied both between sites (F=20.3; df=5, 825; P<.OOl), between years within sites (Table 3-2), and even within one site in the same year (chapter 2). Most of this mortality appeared to have no herbivore related cause and was probably a result of pollination failure or resource limited ovule abortion by the plant. A smaller proportion of ovules (8.89%) failed to mature into viable seeds once they had begun to develop (95% CI: 8.5-9.9% of all ovules). A par~ of this mortality was a result of herbivory which will be discussed below. The failure of an ovule to complete its development was relatively low and constant but there were still significant differences between sites (one-way ANOVA: F= 7.57; df=5, 825; P<.OOl). Table 3-2. Seed mortality in Prosopis velutina in six sites over three years. Values are means. The ~umber of pods per tree includes trees that produced no pods, in order to give an estimate of overall pod product10n levels per site. F-values from one-way ANOVA and significance levels are given below the data. SITE YEAR # of PODS ovules 3 per examined (dissected) pod pods 3 per tree % SEEDS LOST TO # SURVIVING SEEDS % OVULES 1 per per lllC. no 2 4 3 develop. develop. herbivore moths bruchids pod plant 1981 1982 1983 MEAN 228(34) 100{100) 273(40) 13.7 16.2 14.9 14.9 2200 2035 1082 1772 16.9 86.0 11.6 38.2 4.6 3.2 15.1 7.6 1981 1982 1983 MEAN 127(30) 60(60) 150(30) 12.3 15 .1 14.0 13.6 704 1032 847 861 15.9 50.3 13.1 26.4 10.0 15.1 15.3 13.5 1981 1982 1983 MEAN 31(31) 50!50l 181 31 10.8 15.9 14.6 13.6 88 394 212 231 35.5 27.8 U.4 24.9 3.2 5.5 3.6 4.1 6.0 6.0 1981 1982 1983 MEAN 100{100) 90(30) 17.1 17.2 14.1 710 112 411 43.0 43.2 43.1 ll.5 10.1 10.8 0.4 0.4 5 1981 1982 1983 MEAN 74(40) 60(60) 250(40) 11.4 16.1 15.3 14.3 219 1374 335 643 17 .o 23.5 6.8 15.8 6 1981 1982 1983 MEAN 58(28) 80(80) 191(40) 15.6 15.8 15.1 15.5 5149 3891 996 3345 18.5 13.4 14.1 15.3 F df 1981 - 10.0*** 4,512 - 5.4*** 4,164 8.7*** 4,164 1.2NS 3,343 14.8*** 4,512 3.2* 4,37 F df 1982 - 2.4* 5,444 - 24.9*** 5,444 9.0*** 5,444 - 5.3*** 5,444 23. 9*** 5,47 F 1983 - 8.5*** 5,1129 - 16 .8*** 5,205 3.44** 5,205 22. i*** 5,918 13.1*** 5,1129 2.7* 5,46 ALL YEARS - 22.5*** 5,2097 - 20.3*** 5,825 7.5*** 5,825 12.5*** 5,1266 19.5*** 5,2097 3.9** 5,141 2 3 4 df F df 5.4 1.8 7.8 5.0 9.5 0.77 8.7 6.3 8.3 1.1 8.1 5.8 18260 2548 8764 9857 13.7 0.6 13.2 9.2 5.1 1.3 6.1 4.2 6.5 5.0 7.2 6.2 4555 6593 6078 5742 12.5 2.6 8.6 7.9 5.1 5.3 9.8 6.7 4.7 8.5 8.8 7.3 415 4704 1866 2328 - 1.0 10.6 5.8 1.7 5.0 3.4 7.4 5.3 6.4 5583 594 3088 24.9 5.2 7.1 12.4 4.9 1.1 5.9 0.4 4.9 3.7 5.9 7.3 7.1 6.8 4.7 9.3 11.2 8.5 1029 12358 3742 5710 8.5 6.9 7.2 7.5 5.4 3.7 2.9 7.6 4.7 7.9 3.3 11.9 7.7 8.7 11.5 8.9 9.7 44982 57102 8821 36968 2.9 - 2.5 2.7 2.7 - 1.0 1.6 - - 1.6 - 0.6 1.4 *- P<.05; ** p <.01; *** P< .001; 1 Based on data from dissected pods only. 2 Based on data•from visually observed pods only. 3 Based on total data. 4 Based on emergence data. 'I N 73 Predation Related Ovule and Seed Mortality Lepidoptera, Hemiptera, Curculionidae, and Orthoptera all act as herbivores in mesquite in the Southwest (Kingsolver et al. 1977, Johnson 1983). In this study the curculionids were not apparent as important external feeders but Hemiptera were locally abundant, with densities up to 10 per pod in 1982, when pods were abundant. these herbivores were virtually absent. In 1981 and 1983 These fluid-feeding insects mainly suck nutrients from the pod and developing seeds (Kingsolver et al. 1977) and either kill the seed outright or cause it to be aborted. Damage by these kinds of herbivores was indistinguishable from plant initiated ovule abortion discussed above. In contrast, chewing insects leave a distinct record of the number of seeds they have eaten or caused to be aborted, by the damage done to the pod structure. This type of mortality was divided into that caused by unidentified herbivores and that caused by Lepidoptera (mainly Olethreutidae: Ofatulena duodecemstriata (Walsh)). Unidentified herbivores destroyed up to 84% of the seeds in some pods but the overall level of damage by this group was very small (95% CI: 2.06-2.78% of all ovules). Unidentified herbivory was greater in 1981 than in 1983 (3.29% vs 2.1%; T=2.87, df=1269, P<.005) and was higher at site 3 than in all other sites. Lepidoptera ate pod material, ovules and mature seeds, but the majority of their damage was to ovules and immature 74 seeds (Table 3-3). An average of one seed per pod was destroyed or damaged as a result of feeding by Lepidoptera (95% CI: 6.22 - 7.11% of all ovules), but damage was actually quite clumped, with up to a mean maximum of 58.8% of seeds per pod being destroyed in some pods. Moth damage was lower in 1982 (a good pod year) than in 1981 and 1983 (oneway ANOVA: F=74.1; df=2, 2099; P<.001)(Table 3-2). The largest group of seed predators consisted of a guild of bruchid beetles which ranked in order of abundance were; (1) Algarobius prosospis (LeConte), (2) Mimosestes amicus (Horn), (3) Neltumius arizonensis (Schaeffer), and (4) Mimosestes protractus (Horn) (chapter 4). These species mainly attacked mature or almost mature seeds and all four species combined, destroyed even fewer seeds than the Lepidoptera (95% CI: 5.36 - 6.88% of all ovules). Destruction ranged as high as 88% of the total number of seeds in a pod, although it was usually much less. In 1982, sites 3 and 5 had higher bruchid predation than all the other sites. In the poorer pod production years, 1981 and 1983, there were no differences between sites. Differences also occurred between years within the same sites (Table 3-2). Two-way analysis of variance of predation by moths and bruchids by site and year showed a year effect, site effect and year-site interaction for bruchids but for moth predation only the year effect was significant (Table 3-4). Table 3-3. Stage of ovule or seed attacked by Lepidoptera and Bruchidae in Prosopis velutina. Values are the percent of insects in each seed class. MATURING PODS ovules imm. seeds Moths Bruchi ds MATURE PODS mature seeds 50.0% 49.0% 1.0% 0.1% 10.5% 89.4% -...J U1 76 Tab.le 3-4. Two way analysis of variance of bruchid and moth emergence by site and year. A. BRUCH IDS p Source of Variation Sum of .Sguares. Between Treatments 19569 7 2795 11.7 0.000 Site 5449 Year 12083 Interaction 10806 5 2 9 1089 6042 1201 4.6 25.3 5.0 0.001 0.000 0.000 Degrees of Mean Freedom Sguare Error 31057 130 239 Total 61433 146 420 B. F LEPIDOPTERA Source of Variation Sum of Squares Between Treatments 25.95 7 8.68 16.92 6.66 Site Year Interaction Degrees of Freedom Mean Square F p 3.71 2.5 0.018 5 2 9 1. 74 8.46 0.74 1.2 5.8 0.5 0.319 0.004 0.868 Error 190.3 130 1.46 Total 222.88 146 1.53 77 Variation in Seed Production and Predation by Bruchids Individual trees in the same site or even adjacent to each other exhibited distinctly different levels of seed predation. Three out of six sites showed a significant correlation of predation with individual tree (Table 3-5). This variation in attack rate within a population strongly indicates variation in resource quality between trees even within the same population. All the remaining variables with which predation by bruchids was correlated (Table 3-5) deal with either the environment (rainfall in April through July, see chapter 4), or with factors associated with seed quality and the variability in seed quality within a tree or population. Bruchid seed predation was correlated with: (1) the number of good seeds per pod (r=0.356), (2) the number of ovules failing to initiate development (r=-0.374), (3) the number of ovules failing to complete development (r=-0.156), (4) the percent of ovules failing to start or complete development (r= -0.458), (5) the number of good seeds per tree (r=0.189) and (6) the percent of seeds per pod that are good (apparently viable) (r=0.426). The main significant variables deal not with the total number of good seeds per tree or per site but with the proportion of seeds per pod or per tree that was good or bad (Fig. 3-1). There was a very strong significant positive relationship between the percent of seeds destroyed by bruchids and the percent of good seeds 78 Table 3-5. Pearson's correlation coefficients of number of bruchids emerging from seed pods with each factor in six populations of Prosopis velutina. FACTOR SITE 1 SITE 2 SITE 3 SITE 4 SITE 5 SITE 6 .104 SITE YEAR ALL SITES -.308 -.404* -.001 .592* .037 .224 .090 .592* .179 .188 .389*** RAINFALL .586*** .455* .145 MEAN NEAREST NEIGHBOR DISTANCE .023 .111 -.511* -.290 -.211 -.352 -.131 TREE SIZE -.051 .240 .150 .370 -.136 .179 .035 PODS/TREE .008 -.035 .012 -.189 .236 .121 .003 PODS/m3 .058 -.202 -.303 -.667* .224 -.081 -.099 GOOD SEED/m3 .496** .119 -.054 .006 .237 -.098 .132 GOOD SEED/TREE .433** .222 .012 .237 .202 -.130 .189* OVULES/POD .132 -.101 .018 .186 .134 -.188 NO. GOOD SEED/pod .663*** .334 .249 .465 .022 -.164 -.032 . 356*** NO. SEEDS FAILING TO COMPLETE DEVEL. -.084 -.132 -.198 -.163 -.059 -.246 NO. OVULES NOT DEVELOPING AT ALL -.456** -.436* -.569** -. 466* .167 .175 -.374*** .277 .177 .407 -.004 -.285 .307*** -.615*** -.507* -.612** -.521* .011 .041 -.458*** % GOOD SEEDS PER .594*** .479* .434* .520* -.032 -.082 .426*** TREE .141 .555** .492* .194 .320*** NO.OVULES STARTING DEVELOPMENT % OVULES NOT DEVEL. TO MATURE SEEDS .561*** - .156* POD OR PER TREE .005 .398* Fig. 3-1. The percent of seeds killed by bruchids in relation to the total number of good (apparently viable) seeds produced per tree in six populations of mesquite over a three year period. There was no significant relationship between the total number of good seeds per tree and the number of those seeds that were killed by bruchids. ~ 1.0) 80 per pod (Fig. 3-2), indicating that variability in resource quality may strongly limit seed predation by bruchid beetles on mesquite. To further examine this effect of variation on seed predator~. I divided all trees into groups depending upon seed production (high numbers of pods with a high proportion of good seeds (good production) versus low number of pods or with a low proportion of good seeds (bad production)) and synchrony of pod-seed production (whether pod or seed production during the previous year was good or bad). Trees that produced high numbers of pods and good seeds had a greater number of seeds killed by bruchids (high = 29.6 + 1.74SE vs low= 19.7 + 3.4; T=2.88, df=141, p<.005). previous year•s seed production was good, bruchid If the ~redation was lower than if the previous year•s pod production was poor (good = 19.5 ~ 4.26SE vs poor = 34.7 + 2.47SE bruchids/30 pods, T=3.04, df=62, P=.003). This last result was most likely a result of alternate year production patterns. If the previous year was good then the present year will usually be poor in seed production and seed predation will also be poor. To get around this, I further divided the data into three subgroups. If the previous year•s seed production was good and the present year•s production was also good (two good years in a row), bruchids destroyed more seeds (25.5 ~ 4.31) than in the second year of a good year to bad year sequence (16.2 ~ 6.11; T=1.05,df=29,P=.304) but not significantly so. However, in .14 0 (./) 0 I u .10 0 :::::> 0:: 0 0 0 en >- 0 (I) 0 w .06 _j _j 0 :X:: (./) 0 0 w w (./) .0 2 0 0 0.2 0.4 0.6 0.8 GOOD SEEDS Fig. 3-2. The proportion of good seeds produced by a tree was a strong determinant of the porportion of mesquite seeds that were killed by bruchid beetles. Bruchids were negatively affected by a low proportion of good s2e~s per pod on a tr:e. The r:gression equation is: Y = 0.119X - 0.017, r - 0.585, F(1, 15) - 21.1, P- .001. co ,_. 82 a bad to good sequence of years, bruchid seed predation was significantly higher than in a good to bad sequence (34.02 + 2.92 vs 16.2 ~ 6.11) and non-significantly greater than in a good-good series of years (Scheffe multiple range test, P<.05; ANOVA, F= 4.704; df=2, 58; P=.013). To further determine the effect of alternate year production strategies of mesquite on bruchid populations, I placed cages containing mature mesquite pods in a population in which no pods were present. The five test cages had almost four times as many seeds destroyed by bruchids as either an adjacent population in the same year (cages = 3.95 + 0.673SE bruchids/pod vs CR north population = 1.17 ~ 0.096/pod) or the same population in the previous year (1.081 ~ 0.153 bruchids/pod in 1982; T=5.83, df=14, P<.001). Key Factor Analysis: The Relative Influence of Factors on Seed Survivorship Eight factors reduced reproductive output of Prosopis velutina. Table 3-6 expresses these mortalities as percentages of the racemes or ovules lost out of those which survived the previous stage. The largest measured source of loss was due to the failure of mature inflorescences to set fruit (59% of racemes failed to initiate fruit). Since each raceme has approximately 188 flowers, a tremendous number of ovules and potential seeds were lost at this stage. The abortion of immature inflorescences was second (49% of all immature racemes failed to reach flowering stage). There may also be a large number of immature pods aborted, but Table 3-6. Key factor analysis of flower, ovule and seed mortality in six populations of Prosopis velutina over a three year period. 1983 1982 FACTOR MEAN1 SLOPE MORT. IMMATURE RACEME DROP .438 2.73 5.2* P=.OS -- MATURE RACEME DROP .590 1.40 .981 158.1* P=.001 IMMATURE POD ABORTION . 700 (est.) - r2 .638 - 1981 r2 F - - - - - - - - - -- - - - F MEAN1 SLOPE MORT. MEAN OF 1981 - 1983 r2 F - - - - - - - - - - - - MEAN1 SLOPE MORT. r2 F DENSITY DEPEND. - - - No - - - - Yes - - - - ? .421 2;2 .271 P=.24 1.12 .354 1.6 .085 2.38 P=.29 .097 1.6 No P=.15 MEAN1 SLOPE MORT. NO DEVELOPMENT OF OVULES .174 1. 52 .908 39.4* .407 1.20 . 995 807. 0* . 203 0.96 P=.003 P=.001 HERBIVORES .026 -3.19 .077 MOTHS .111 4.95 .837 20.5* .039 14.22 P=.Oll . 744 INCOMPLETE SEED DEVELOP. .126 2.69 .591 5.8* .167 4.52 P=.07 .516 4.3 P=.1 .503 .167 0.6 P=.S .144 2.81 .365 8.6* No P=.01 BRUCH IDS .129 2.66 .087 0.4 .066 5.03 P=.57 .038 0.2 .111 -3.15 P=. 7L .123 0.4 .102 -.172 P=.56 .018 0.3 No P=.61 1 * .938 228.0* No P=.001 0.3 P=.59 11.6* .108 1.32 P=.027 .139 Mean mortality - the number of racemes or ovules lost after the action of all previous mortality factors. Indicates significant key factors. CX> w 84 since sample sizes for this factor were small, it was not included in the analysis, even though up to 70% of immature pods (newly formed less than two weeks) may be aborted (see chapter 2). Once pods have been formed, seed mortality was mainly a result of the failure of ovules to initiate development (27.1% of all ovules), and the incomplete development of seeds (12.4 % of all zygotes that started failed to complete development). The remaining predation related factors were less important (bruchids 10.2%, moths 8.5%, and herbivores 2.6%). The relative contribution of each factor to potential seed mortality in these populations of mesquite was examined using key factor analysis. Heithaus et al. (1982) modified key factor analysis techniques for the examination of variation in subpopulations in space instead of the usual analysis of one population through time (Varley et al. 1974, Podoler and Rogers 1975, Manly 1978). I used the method of Heithaus et al. (1982) to examine the relative importance of reproductive mortality in six populations of mesquite over a three-year period. In this analysis, the losses due to factor k 1 are regressed on total losses K, with different sites and years all as replicates: k; = log 10 N(i-1)- loglO N; (1) and K = k1 + k2 + k3 + ••• + kn where Ni is the number of ovules or racemes present after 85 3 0 ~ 0 K 2 o· ~k2 ~ 0~ >- 11- ~ a: ~ ok1 0 /0 / o---- o-- 0~<>~ ....J <( 0 o~ 0 0.1 k3 o-~~ ·~:-K•7f_:\ Q 0 ~ k7 Bks ~ k4 ~ 0 3 2 4 5 SITE Fig. 3-3. Key factor analysis of reproductive mortality in five populations of Prosopis velutina in 1983. K - total mortality; k1 - preflowering raceme loss; k2 - post-flowering raceme loss; k3 - loss due to the failure of ovules to initiate development; k4 - loss due to predation by Lepidoptera; k5 - loss due to the failure of seeds to fully deve 1op; k7 - loss due to predation by four species of bruchids; k6 - losses due to herbivores were very minor and were not included. 85 .5 0 0 .4 0 ~ .3 >- f_J 0 <( f- Q a: 0 ~ 0 .2 Q---- ~OK Q .1 2 3 4 5 6 SITE Fig. 3-4. Key factor analysis of post-flowering reproductive mortality in six populations of P. velutina over a three year period. K - total mortality; k3-- loss due to the failure of ovules to initiate development; k4 - loss due to predation by ~epidoptera; k5 - loss due to the failure of seeds to fully develop; k7 - loss due to predation by four species of bruchids. 87 the effects of factor i (Podoler and Rogers 1975). The analysis was broken into two sections, with flowering based upon raceme mortality (the functional flower unit) and seed production based upon the total number of ovules per pod. A slope, r2 and F-values are presented for each regression for all sites 1981 through 1983 and for all years combined (Table 3-6). If the F-value for the regression was not significant the slope that is shown is not significantly different from zero and there is no reliable relationship between K and ki. If the regression F-value is significant the slopes and r2 values may be used to compare the relative influence of each factor, with larger slopes indicating a greater influence of k; on K. In 1981 there were no clear key factors, but the incomplete development of ovules was most significant when examined graphically (4/5 of all points show a strong linear relationship). In 1982 and 1983 the failure of ovules to initiate development and predation by Lepidoptera and in 1983 mature inflorescence abortion were the major factors explaining variation in reproductive output among the different years and populations (Fig. 3-3 and 3-4). DISCUSSION Fruit and seed production in mesquite populations appear to be more a result of environmental and resource limitation than a coevolved interactive system of seeds and seed 88 predators. In chapter two, I clearly demonstrated that flower and immature fruit development entails very little relative investment costs compared to the investment in a mature fruit with mature seeds, although the greatest cost per unit time (in terms of water and respiratory expenditures) is invested during these early flowering and fruiting stages. The basic reproductive strategy of mesquite thus appears to be a type of bet-hedging in which each tree almost always attempts to reproduce maximally but then restricts the number of fruits and seeds that it eventually matures based upon an allocational strategy by the individual plant. There is a definite cost involved in such a strategy (Stephenson 1984) but in mesquite in a harsh unpredictable desert environment evidently the benefits outweigh the costs. The abortion of (1) inflorescences after they have flowered but before setting fruit, (2) inflorescences prior to flowering, (3) newly-formed immature pods, and of (4) ovules, all of which are the predominant losses in potential reproductive output in mesquite in this study, thus are relatively inexpensive in comparison with the potential gain that might be achieved if conditions for reproduction are optimal in a given year. These stages all occur during the harshest period of the year, between April and July, when rainfall is minimal and temperatures are extreme. Trees may be severely stressed by environmental conditions during the period of production of flowers, pollen, nectar, and 89 immature fruits. However, the tree may be constrained to begin reproduction during this period by even stricter requirements for seed germination and seedling survival (Dafni and Negbi 1978, Meyer and Bovey 1982, Scifres and Brock 1969, 1972, Tschirley and Martin 1960, Ueckert et al. 1979). While some of this early mortality may be a result of pollen limitation and herbivory of flowers, inflorescences and ovules, other studies have indicated that these factors may be of little significance (Willson 1983, Simpson et al. 1977, Dafni and Negbi 1980). The abundance of pollinators on mesquite in this study and the high levels of pollen and nectar produced by Prosopis velutina (Simpson et al. 1977) seem to decrease the probability of pollen limitation playing a major role in reproductive mortality, although selection for specific pollen-ovule combinations (pollen quality) is highly likely in a selective abortion process (Willson 1983, Heithaus et al. 1982). Flower and ovule feeding Coleoptera and Thysanoptera were sometimes abundant on inflorescences in these populations of mesquite but no ' quantitative measure of the damage caused by these insects was attempted. The relative importance of these flower-feeding insects as a potential cause of flower and raceme abortion needs further study. Whatever the causes, these early losses result in the greatest decrease in reproductive output. Therefore, these factors will be the most likely to influence (or have influenced) the evolution of reproductive strategies in mesquite. 90 Since Janzen's (1969) seminal paper on the importance of seed predation as a potential selective force on plant reproduction, many systems have been examined. Seed predators and especially specialists like bruchid beetles, have been implicated as potent evolutionary forces acting on plants resulting in a very tight coevolutionary link between the two trophic levels (i.e., via the Red Queen hypothesis, Van Valen 1973, Center and Johnson 1974, Green and Palmblad 1975, Hare 1980, Johnson 1981a, Johnson and Slobodchikoff 1979, Moore 1978a, Janzen 1977, 1983, Solbrig and Cantina 1975). However, the majority of these studies have examined only seed predation and often only one group of potential seed predators. Examination of the data in these studies shows that seed predation is not consistently the potent evolutionary selective force that had been hypothesized. Seed predation levels range from very low (Janzen 1969, Johnson and Slobodchikoff 1979, C. D. Johnson pers. comm.) in a majority of systems to as high as 100% in a few cases (Janzen 1969). High levels of seed predation need not mean that seed predators are important agents in plant evolution. Janzen (1978) hints that other factors might be important selective agents in plant reproductive strategies but he still fails to determine the relative importance of bruchid seed predators in the evolutionary dynamics of the host plants. Only one other study (Heithaus et al. 1982) has intensively examined the multitude of factors that might influence flower and fruit production in a plant species. 91 They examined five populations of Bauhinia ungulata (Leguminosae) and found that seed predators were fourth out of six factors that affected reproductive output. In sharp contrast to all of these studies the present study on mesquite intensively examines differential seed mortality over a three-year period. Even Heithaus et al. (1982) was only a one-year study in which they assumed that relative mortality levels remained constant between years. This seems unlikely and is certainly not supported by the data presented in this study. I have also examined levels of flower production prior to seed set for one year to determine relative decreases in potential reproductive output at each stage of reproduction.(with qualitative data for two more years). Herbivorous chewing insects destroyed only 0.41 to 6.0% of all ovules, seed- and pod-eating Lepidoptera resulted in the direct or indirect death of 0.42 to 13.2% of all ovules, and the bruchid guild destroyed only 0.77 to 11.9% of all ovules in any population over the three years of the study. Thus, although individual trees were attacked to a greater extent, the overall effect of insect caused seed mortality within a population appears to be relatively unimportant. The results of the key factor analysis indicated that the relative importance of the ovule-seed mortality factors varied dynamically from year to year. In 1981 and 1983, immature and mature inflorescence abortion was predominant at some sites, while in 1982 these two factors accounted for 92 a much lower proportionate decrease in reproductive output. The failure of ovules to develop and mortality caused by moths were respectively the two most significant key factors in 1982 and 1983, but in 1981 no factor explained a significant amount of the variation in mortality among the populations. Over all three years seed predation failed to explain any significant amount of the spatial and temporal variation in total losses in potential seed production, while the failure of ovules to initiate or complete development were significant key factors. Therefore, at least in the Verde Valley of central Arizona, bruchid beetles and probably all seed and pod predators and herbivores should have_ very little, if any, influence on the reproductive output of Prosopis velutina. As potential evolutionary forces it appears that these insects hold little or no selective sway over mesquite populations. Several other studies have shown relatively high levels of seed destruction by bruchids in mesquite (Glendening and Paulsen 1955, Kingsolver et al 1977, Johnson 1983). However, closer examination of either the data or the collection and rearing techniques used shows that these studies may have exaggerated the importance of bruchids. Solbrig and Cantina (1975) examined damage by bruchids in 15 species of Prosopis and found that only a mean of 10.5% of all ovules were destroyed (range 1-25%), while 17.1% of all ovules were underdeveloped (range 7- 25%). Glendening and Paulsen (1955) have shown that up to 80% of the seeds may be 93 destroyed by bruchids if the pods remained undispersed under the parent tree, but predation levels were very low (<10% of all ovules) for over two months after the pods had reached maturity. Many or most of the pods of mesquite are dispersed within this time period and removed from predation, and so after this time predation rates would only be expected to rise dramatically because of the smaller resource pool for bruchids to attack. Thus, most maximum estimates of bruchid predation may be a result of this resource concentration as pods are dispersed. This is indicated in the data of Janzen (1969), Solbrig and Cantina (1975), and Glendening and Paulsen (1955), although in some cases the loss of major dispersal agents may have increased the apparent importance of bruchid beetles in contemporary time to the point where they might be potentially important selective agents. The methods used in this study minimized the effects of dispersal and resource concentration, by using mean emergence levels of bruchids throughout the season). This provided more accurate estimates of the true population levels of bruchid seed predators. Therefore, in reality, most studies of mesquite indicate that bruchid beetles destroy relatively few seeds and that other factors may usually be more important than these seed predators. The variability within and between pods, trees and populations may, however, have a significant effect upon bruchid populations. Bruchid predation shows no density dependent relationship with the total number of resources 94 within a population, but does show a significant relationship with measures of resouce quality within a population (Fig. 3-2). Also in contrast with other studies that show an increase in seed predation in years of poor seed production, due to a numerical response in good years (DeStephen 1981, 1982, Sork 1983) and a decrease in predation in years of high seed production (mast species; Janzen 1976, Silvertown 1980) due to predator satiation, this study indicates the opposite. In good years seed predation is higher than in years of poor seed production. Similarly, if a tree produces a large number of pods and seeds two years in a row, the number of seeds destroyed by bruchids does not increase significantly, indicating a relatively constant level of bruchid populations. The low level of attack in years of poor pod and seed production, followed by a higher level of attack in years of good pod and seed production, may indicate that bruchids limit oviposition in a poor resource year instead of attempting either to emigrate to another mesquite population or to waste energy and eggs attempting to locate a few good seeds in a very heterogenous environment of pods with a low percent of good seeds. This strategy correlates well with life history data presented in a previous paper (Kistler 1982) and in chapter 4. Some Mimosestes amicus, the second most abundant member of the bruchid guild on mesquite, will often not oviposit on pods in the laboratory and as a result may live for a very long period of time (> 200 days at 35 95 C). Those that oviposit freely live a much shorter period. The high levels of bruchids found in a population without pods, in the cage study and the lack of a difference in seed and pod predation by Lepidoptera, which act mainly as herbivores and not obligate seed predators, all support this idea. This is, however, only one explanation for the higher attack rate in good years. Such a strategy would entail a physiological cost (decreased reproductive output in second year bruchids) and a potentially large mortality cost due to predation (Kingsolver et al. 1977), but would explain the relative constancy of population levels in mesquite bruchids in spite of alternate year pod production and widely separated populations of mesquite. Another possiblity is that in good pod years dispersal of seeds and pods takes longer (satiates dispersal agents) allowing a greater buildup of bruchid populations. This, however, fails to explain why population levels would be higher in a bad to good year sequence than in a good to good year sequence of pod production. Variation in seed quality and variation in seed and pod production thus seems to strongly limit populations of bruchids and their potential to act as selective forces on mesquite reproductive strategies. Of course these strategies might be an evolutionary response to intense seed predation pressure by these bruchids in the evolutionary history of mesquite. Janzen (1975,1978) hypothesized that such is the case in Hymenaea courbaril in Costa Rica, but 96 such ideas cannot be tested and it seems that if bruchid predation is minor today in the absence of many coevolved dispersal agents (Janzen and Martin 1982), then the evolutionary importance of bruchi.ds in the past seems unlikely. Perhaps for these reasons we should begin to look away from seed predators to other factors for an explanation for many plant reproductive strategies. Another alternative hypothesis which might explain levels of seed predation by bruchids is that bruchid populations are regulated by a third trophic level of parasitic Hymenoptera. In the present paper all larval parasitoids were included as a part of the total bruchid predation. However, trichogrammatid (Hymenoptera: Trichogrammatidae) egg parasites destroyed a large number of the eggs laid by all members of the bruchid guild (chapter 5). If parasitoid populations are more adversely affected by alternate year pod production, this could explain the differences between seed predation between years of good and bad pod production. After a good year, parasitoid population levels should be higher and so bruchid populations would be lower in a subsequent poor pod production year. Then in a subsequent good pod year bruchid populations might be released from parasitism due to a poor parasitoid numerical response the previous poor pod year, and the resulting seed predation by bruchids would be much higher. This possibility is improbable based on data presented in chapter 5, but there is a strong possibility 97 that these populations of bruchids might be strongly regulated by parasitoids (Kistler 1979, 1985). Janzen (1969) and Center and Johnson (1974) describe numerous traits of the Leguminosae and coadaptations of their seed predatars that may function to either decrease the level of bruchid attack on the seeds of a plant or conversely allow the bruchid seed predators to counter the plant's anti-seed predator strategies. Twelve of the 31 traits mentioned by Janzen are found in Prosopis velutina and four of these 12 traits deal with timing and synchrony of pod production as methods to decrease bruchid predators. ~eed Neither of these papers, or for that matter many other studies of seed predator-plant interactions, have actually demonstrated that these are actually coevolved responses of the two trophic levels as is implied in these works (for possible exceptions see Bradford and Smith 1977, Green and Palmblad 1975, Hare 1980, Hare and Futuyma 1978, Janzen 1975). However, even in those studies that demonstrate that seed predators and their hosts might have evolved coadapted responses to decrease seed predation or void plant defenses, for the most part they have all failed to show the importance of seed predation relative to other potential plant reproductive mortality factors, which might counter or override evolutionary responses to bruchids by the host plant. This study of Prosopis velutina and its diverse guild of at least five seed predators (four bruchids and at least one lepidopteran) clearly demonstrates that at 98 least at the present time these seed predators do not exert a strong selective pressure on plants and their reproductive strategies. In these populations of mesquite reproduction was more strongly influenced by flower abortion (resulting from pollination processes, herbivores, and environmental parameters), and ovule abortion (again related to pollination, environmental or plant resource parameters). Conversely, evidence is presented that reproductive strategies of mesquite do negatively affect populations of bruchids and possibly of their parasitoids as well. These data provide evidence that immature fruit and seed abortion may, in opposition to a statement by Janzen (1983), actually act as a direct defense. The plant can lower the intensity of seed attack by greatly increasing the variability faced by seed predators in searching for host seeds capable of supporting the development of these specialized seed predators. 99 LITERATURE CITED Bradford, D.F. and C.C. Smith. 1977. Seed predation and seed number in Scheelea palm fruits. Ecology 58:667-673. Carter, M.G. 1964. Effects of drouth on mesquite. J. Range. Manage. 17:275-276. Clark, D. A. and D. B. Clark. 1984. Spacing dynamics of a tropical rain forest tree: evaluation of the Janzen-Cannell model. Am. Nat. 124:769-788. Center, T. D. and C. D. Johnson. 1974. Coevolution of some seed beetles (Coleoptera:Bruchidae) and their hosts. Ecology 55:1096-1103. Dafni, A. and M. Negbi. 1978. Variability in Prosopis farcata in Israel: seed germination as affected by temperature and salinity. Isr. J. Bot. 27:147-159. Dafni, A. and M. Negbi. 1980. 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Reproductive adaptations in Pr.osopis (Leguminosae,Mimosoideae) J. Arnold Arb. Harvard University. 56:185-210. Sork, V.L. 1983. Mast-fruiting in hickories and availability of nuts. Am. Midl. Nat. 109:81-88. Stephenson, A.G. 1981. Flower and fruit abortion: proximate causes and ultimate functions. Annu. Rev. Ecol. Syst. 12:253-279. Stephenson, A.G. 1984. The cost of over-initiating fruit. Am. Midl. Nat. 112:379-386. Tschirley, F.H. and S.C. Martin. 1960. Germination and longevity of velvet mesquite seed in soil. J. Range Manage. 13:94-97. 106 Ueckert, D.N., L.L. Smith and B.L. Allen. 1979. Emergence and survival of honey mesquite seedlings in several soils in West Texas. J. Range Manage. 32:284-287. Vandermeer, J.H. 1974. Relative isolation and seed predation in Calliandra grandiflora, a mimosaceous legume from the highlands of Guatemala. Biotropica 6:267-268. Van Valen, L. 1973. A new evolutionary law. Evol. Theory. 1:1-30. Varley, G.C., G.R. Gradwell and M.P. Hassell. 1974. 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CHAPTER 4 The Effect of Temperature on Mesquite Bruchids (Coleoptera): Physiological ~trategies of a Guild of Seed Predators 107 108 INTRODUCTION The recent deemphasis of competition as an important organizing factor in ecological communities (Lawton and Strong 1981, Simberloff and Connor 1981, Wiens 1977) has prompted ecologists to search for alternative factors that may play a role in community organization. overlap is common in insect communities. High resource However, insects are small and short lived, highly sensitive to spatial and temporal variation, and their populations are rarely at equilibrium. Thus, competition is less likely to ~e an effective selective force in these communities (Rathcke 1976). Studies of community interactions indicate temperature and other major abiotic variables to be very important factors in insect community interactions. Two coexisting populations of featherwing beetles (Ptinella) in Southern England are distinguished mainly by differential temperature adaptations, due not to competitive niche separation but to evolution in different environments (Taylor 1980). The outcome of competition between two species of Tribolium can be reversed by changing temperature and humidity conditions (Park 1954). Two species of stored product Bruchidae are similar, in that competitive extinction of two species of Callosobruchus is determined by ambient temperature (Fujii 1967). Eggs of two species of Bruchidae, Mimosestes amicus (Horn) and Stator limbatus( .Horn), which attack seeds of 109 Cercidium floridum Bentham (Leguminosae), are adversely affected by environmental stresses. Abiotic factors may be strong determinants of oviposition strategies in these two beetles (Mitchell 1977). In a community of water striders (Gerridae) the differential effects of temperature influence the community through effects on developmental rates and fecundities of the component species (Spence et al. 1980). Microgeographic races of a coastal dune beetle, Coelus ciliatus (Tenebrionidae), differ in temperature preferences, population density and body size due to adaptation to different environmental regimes (Doyen and Slobodchikoff 1984). Temperature relations of four species of Stator (Bruchidae) closely correspond to the feeding guild (Johnson 1981b) to which each species belongs (Kistler 1982). These and other studies implicate the importance of temperature to insect populations (Clarke 1967, Mutchmor 1967, Bursell 1964, May 1979, Keister and Buck 1974). All these studies suggest that insect community dynamics might be strongly regulated by the abiotic environment, limiting the potential for inter- and intra-species interactions and perhaps even limiting coevolution with host plants. Thus niche differences between sympatric species sharing the same· resource might be due, in large part, to different evolutionary responses to physical differences in the environment. Four species of seed beetles (Coleoptera:Bruchidae) Algarobius prosopis (LeConte), Mimosestes amicus (Horn), 110 Mimosestes protractus (Horn) and Neltumius arizonensis (Schaeffer) attack the seeds of mesquite, Prosopis velutina Wooten in Arizona. Three of these species feed only on the seeds oft. velutina, hosts. ~· while~· amicus uses several alternate prosopis is the most abundant species and has been hypothesized to have been the selective agent (via competitive interactions) responsible for the observed community structure. The other species have been selected for temporal or spatial displacement in order to coexist with this dominant species (Swier 1974, Kingsolver et al. 1977, Pfaffenberger and Johnson 1976). The objectives of this study were to assess the degree of similarity of the physiological responses to temperature variation which, since these are desert-adapted populations, may potentially play an important part in the population dynamics and coexistence of this guild of seed predators. Since these four species feed on the same resource at roughly the same times and have comparable ranges, they could be expected to have very similar physiological capabilities, with regard to body size, water relations, host utilization efficiencies, fecundity, and responses to temperature. Temperature was singled out as an important variable because it is the most variable and prominent factor in desert ecosystems and other parameters (i.e., water) are an inherent part of the bruchid-seed self contained ecosystem. utilization. Selection should be for optimal host Differences could be attributed to 111 differential adaptation (divergent evolution) to a similar environment based on genetic, ecological and evolutionary constraints in each species and need not be due to competitive divergence. The questions being addressed are; (1) Are these bruchids limited by the abiotic environment? (2) If so, are there differences in the responses of these four species to environmental variables which might explain their abundances and differential host utilization patterns? These questions will be assessed by examining the comparative physiological ecology of the mesquite bruchid guild and the resulting evolutionary strategies of the member bruchid species. Bruchid beetles are highly specialized seed predators attacking seeds mainly in the family Leguminosae (Johnson 198la). The species in the mesquite guild attack mesquite seeds which are contained inside a woody indehiscent pod. ~· amicus, N. arizonensis and M.protractus females attach their eggs individually to the pod surface, while A. prosopis oviposits either in damaged areas, cracks or crevices on the pod, or in the exit holes formed by either other bruchids or by pod and seed feeding Lepidoptera (Kunhikannan 1923, chapter 5). The larvae of the former species burrow into a seed directly below the egg, while larvae of~· prosopis possess well developed legs and may travel either over the surface of the pod or through the intra-pod matrix to choose a host seed (Pfaffenberger and Johnson 1976). After boring into the seed, the larvae pass 112 through about 5 instars (Wightman 1978b), pupate in the seed, and emerge as a mature adult from the seed. The adults probably feed on pollen and nectar of mesquite and other plants (Kingsolver et al. 1977, Johnson and Kistler 1985). All species in mature pods. except~· ~· protractus mainly attack seeds protractus is morphologically specialized for attacking green-immature pods. Larval thoracic appendages are replaced by decurved spines to aid in entering the soft pods without impeding movement in the sappy pulp of the immature pod (Pfaffenberger and Johnson 1976). M. protractus is an aberrant member of its genus. It is the only member of the Protractus group, and feeds only on two species of Prosopis (Kingsolver and Johnson 1978). This species is the rarest member of the guild but may be locally abundant (Conway 1980). N. arizonensis ·is the second rarest member of the guild. This genus does not appear to be related to any of the other recognized species groupings in the new world. It is restricted to the Sonoran Desert of the United States and Mexico, and is a specialist on Prosopis species (Kingsolver 1964, Johnson 1978). M. amicus is the second most abundant member of the guild. It is a member of the Mimosae group of Mimosestes, which is probably the youngest and most actively evolving group within the genus. It is the only generalist in the guild and feeds on a variety of seeds, mainly species of 113 Acacia, Cercidium, and Prosopis (Kingsolver and Johnson 1978). A· prosopis is the most abundant member of the mesquite bruchid guild. Its oviposition behavior and its mobile first instar set it aside from the other three species in the guild. These traits and larval characteristics are similar to those found in the closely related genus Acanthoscelides (Pfaffenberger and Johnson 1976). Because these traits are found in several closely related genera, they are probably not specific adaptations to the Prosopis ecosystem, although they might very well be pre-adapatations to successful utilization of Prosopis as a resource. METHODS Field Studies Bruchid populations were studied in a population of mesquite near McGuireville in the Verde Valley, in central Arizona. This population is relatively undisturbed and cattle have not been present during the study period. Ten trees were monitored every 7 to 14 days from May, 1981, through October, 1983, and the phenological state of each tree was recorded. After initiation of pod development a 30 pod sample (approximately 450 seeds) was collected at random from each tree every 7 to 14 days. These samples wer~ placed in quart mason jars with paper towel lids and reared in a laboratory culture room at a thermoperiod of 30° 114 C-12h/25°C-12h. All insects that emerged from these pods were removed and counted every 7 days for 50 days. Laboratory Studies All four species were reared from pods of f. velutina collected in the Verde Valley, and with the exception of M. protractus were reared for at least one generation in the laboratory at a thermoperiod of 30°C/25°C on pods from the same tree, to avoid all acclimation responses and host seed differences. li· protractus will not breed in the laboratory and so reared adults were maintained on a 10% solution of sucrose for approximately 30 days prior to the experiment. Temperature ranges were chosen for the experiments based upon climatological data from the Beaver Creek Ranger Station at Rimrock, Yavapai County, Arizona, and from surface and internal temperature measurements of pods using a Bailey thermoprobe. The oxygen consumption of adults of all four species and larvae of all but li· protractus, was measured with a 20-station Gilson differential respirometer, using the method described by Kistler (1982). Ten adults (5 forM. protractus) less than 24 hours old, or approximately 15 larvae (23 days old, 1 larva/seed) in their host seeds were placed in 15-ml respirometer flasks. The larvae were all tested in one experiment and all adults were tested in a second experiment. Respiration (oxygen consumption) was measured at temperatures of 20 to 50°C in 5-degree 115 intervals. Four replicates were used for each species for adults and 5 for the larval trials. Four control flasks were used, consisting of 15 uninfested host seeds per flask for the larval trials or four empty flasks for the adult trials. After the experiments, the adults and the larvae inside the seeds were dried for 48 hours at 60°C. The larvae were then dissected out of the seeds and dried for another 48 hours, prior to weighing. Oxygen consumption was calculated at STPD (0°C, 760mmHg, dry gas) in microliters of oxygen per milligram dry weight per hour. Adult fecundity was determined at four temperatures: 20, 25, 30, and 35°C. Virgin pairs (male and female) were placed in quart or pint jars, with paper towel tops treated with 1% Kelthane to protect against pyemotid mite infestation, along with 20 mesquite pods and a piece of sponge soaked in a 10% sucrose solution. These cultures were placed into environmental chambers maintained at the given temperature and at a humidity of approximately 70%. Pods were replaced and the eggs were counted weekly. Because of the secretive oviposition behavior of A. prosopis, counting eggs of this species was unreliable and so the number of emerging adults was used as the only available estimate of fecundity. Since larval survival was relatively high for all species this should be an accurate estimate of fecundity. After each week the egg-containing pods were placed at 30°C to facilitate larval development. Four or more replicates were used for each species at each 116 temperature. Longevity was also recorded for each beetle used in these experiments. Developmental rates were determined by placing 20 pairs of adults on 30 pods for 3 days at 30°C. Two replicates for each species were then placed at each temperature (20, 25, 0 30, 35 C). The emergence of adults was then monitored daily to achieve an estimate of rate and pattern of emergence. Larval survivorship was also estimated from these experiments. Since all replicates were identical and assigned randomly to each temperature group, the total number emerged at each temperature was divided by the maximum number emerged at any temperature to give a relative estimate of larval mortality at each temperature. Thirty virgin adults (~5 of each sex) and 30 eggs less than 48 hours old, of each species, were weighed, dried at 60°C for 48 hours, and then reweighed on a Cahn electrobalance to determine weight and water content differences between species. All data were subjected to one-way analysis of variance across temperatures for each species and across species for each temperature. Pairwise contrasts and orthogonal contrasts (Scheffe and LSD) were used where appropriate to examine group means. 117 RESULTS The phenological timing of the trees and the bruchid species, and the climatological data are shown in Fig. 4-1. The peak of oviposition (left arrow) for~· protractus clearly indicates strong utilization of green pods. This species is most active during the hottest and driest part of the season and drops out as green pods become unavailable. The oviposition (center arrow) and emergence peaks for~· prosopis and M. amicus are almost totally overlapping and coincide with the peak in mature pod (pods containing mature seeds) numbers. The curve for ~· prosopis is broader, indicating a broad seasonal activity and resource use. Most of these first three species emerge prior to pod fall. N. arizonensis appears to prefer to oviposit on dry (right arrow), mature pods and thus occurs later in the season than all the other species. Temperature and moisture stress have decreased by late summer when this species is actively ovipositing and developing. The phenological timing of two of the four species is thus distinctly different. During these three years, the relative abundance of the four species remained relatively constant (Table 4-1). absolute abundances, 1982. howe~er, The were drastically reduced in This was due to a small proportion of viable seeds being produced (chapters 2, 3), and resulted in the disappearance of the two rare species (Table 4-2). These data not only clearly indicate the numerical dominance of A. 0-0 A ~MA 30 I \ I \ I \ I \ oro~i~ ·a. I w ~20 w t9 0:: w ~ 10 w l l ~ \0 \6, \ AP 1/'o-o o'-'\o ~~, I 6~ 01 1 /6o----- n - - ' ___ o~ ~o ~~ooi FLR _, 8 I / I 5 / c ,' ' DRY ' • ' I ;;_52 ~0 GREEN / 0 \ '-- I ------,' I 1-.. I I ' I 3 ', ' "- I / 15 / "" " "" I I ........ " M J J " I \ I \ I I 0 A ,/ ", .... ,, / I zu~:=~-~--f,.......~~~~~ s --- ' ', I I 0 GRD 25 - \ --@.:-=-::@ ',·6~ I ' // 0 o ~bNA I ' I ' .... --- .... ' ', 0 A 0 N D J Fig. 4-1. The temporal patterns of (A) emergence of the four species of bruchids, (B) phenology of reproducUon in Prosopis velutina, and (C) temperature and rainfall patterns for the study site (Beaver Creek Ranger Station, National Oceanic and Atmospheric Administration, Asheville, N.C.). All figures represent means of three years of data. See text for explanation. t-• 1--' OJ Table 4-1. Relative abundance of bruchids in the mesquite seed predator guild. The ratio of the abundances as well as the percentofeach species in the total bruchid population are given. YEAR RATIO PERCENT A. prbsopi s !1_. amuu-s !!_.- arTzonens1 s M.-protractus AP:NA:NA:MP 1981 91.2% 7.2% 1.01% 0.60% 1982 91.6 8.4 0 0 1983 91.4 7.14 0.50 0.94 238:18:4:1 AP:MA 12.8:1 11.0:1 183:14:1:2 12.8:1 ~ ~ \.0 - . Table 4-2. Numbers of bruchids emerged from 30-pod samples of Prosopis velutina over a three year period. DATE VI-24-81 VII- 7-81 VII-22-81 VIII-3 -81 VIII-12-81 VIII-21-81 IX- 4-81 IX-16-81 IX-26-81 X-10-81 VIII- 3-82 VIII-18-82 VIII-26-82 IX- 1-82 IX-16-82 IX-30-82 X-14-82 X-28-82 XI-20-82 VII-30-83 VI II -13-83 VIII-22-83 IX- 1-83 IX-13-83 IX-22-83 X- 3-83 X-17-83 A. prosopi s MEAN SD 0 4.8 19.2 34.0 24.2 27.0 35.1 33 77.5 20 1 0.5 0 1.44 5.4 4.17 2,75 3.78 5.25 15.7 48.8 33.7 34.6 31.4 40.8 36.9 50.6 6.9 9.6 20.0 10.7 14.5 22.0 57.6 0.7 1,42 5.6 3.83 2.76 2.95 3.40 9.5 22.0 23.0 23.6 13.6 22.3 15.8 25.0 M. amicus MEAN SD N.arizonensis MEAN SD 0 0 1.1 1.4 4.5 10.8 2.8 3.4 2.6 3.0 2.1 3.1 1 1.5 1.0 4 0 0 0 0.07 0.10 0.33 1.12 1 2.5 8 0 0.5 0.7 0 0 0.26 0.44 0 0 0.33 0.50 0 0 0 0 0 0 0 0 0 0 0 2.25 0.45 2.79 1.94 1.87 1.60 2.50 0 0.5 0 0 0.01 0.13 0.30 0.38 0.96 0.69 4.20 2.10 1. 50 1.60 1.80 0.27 0.27 0.85 0.83 3.0 1.0 0.24 0.35 0.48 0.74 M.protractus NUMBER MEAN SD OF TREES 0 1.4 1 0.5 1.0 0.36 0.84 0 0 0 0 0 0 4 5 4 14 20 13 8 1 4 1 0 0 0 0 0 0 0 0 0 1 2 2 8 16 12 8 9 4 5.0 2.0 0 0.27 0.47 0 0.12 0.33 0 0 0 3 4 11 14 17 15 10 8 I-' N 0 121 prosopis and M. amicus in the mesquite guild, but also that all of the species combined only destroy a very small proportion of the total seed crop. Even considering cumulative attack, much less than 33% of all the seeds were destroyed by the bruchids and these infestation levels are much greater than those actually found in the field (chapter 3, 5). Mesquite seeds are thus an abundant resource at all times and are not a limiting resource. The mean monthly temperatures during the period of greatest bruchid activity (July to September) are around 25° C. Diurnally temperatures vary greatly, ranging from 10°C to 40+ C (Fig. 4-2). vary diurnally. Similarly pod and seed temperatures The bruchid larvae thus develop in a constantly changing thermal environment. The internal pod temperatures vary depending upon the phenological state of the host pod (Table 4-3). Temperatures of green pods did not vary significantly from ambient air temperature (T = 0.86, df= 7, P=0.419). Temperatures of dry pods averaged 1.6°C above ambient in full sunlight. The internal temperature of pods on the ground was best estimated by the mean of ground surface temperature and the air temperature 1 em above the ground. The temperature of these pods was buffered to some extent by the soil mass but still reached temperatures as hig~ as 50°C in September. 50 . w 0:: ~30 <( 0:: w 0.. ~ w ..___ 10 TIME DATE 6PM 9-16 6PM 9-17 6AM 6PM 9-18 6AM 6PM 9-19 Fig. 4-~. The daily temperature variation in the lower crown of a mesquite tree for four days in September, 1982. 1-' r.J r.J Table 4-3. Internal temperatures of mesquite pods, for green and dry pods on the tree, and for pods on the ground. pod state description De vi ati on from ambient °C GREEN AMBIENT .500 + .582 DRY t1EAN 0 F SHADE AND SUN 1.594 + .517 GROUND MEAN OF GROUND TEMP AND AIR TEMP AT 1 em 11.19 + 1.86 ....... N w 124 Respiration The metabolic rate in adults of these four species increased significantly with temperature. The rates of increase fall into two groups (Fig. 4-3). The metabolic rates of Mimosestes amicus and~· protractus are only very slightly affected by changes in temperature, while those of A· prosopis and N. arizonensis are affected to a much greater extent, indicating a greater degree of homeostasis in the former. The metabolic rate of M. protractus is lower overall than all the other species at most temperatures, while that of M. amicus is higher at temperatures below 35° C. These re spon s·e.s are simi 1 a r to those that have been reported for other desert bruchid species (Kistler 1982) and for other insects (Keister and Buck 1974). A major difference in the responses of these adults to temperature is the relatively strong negative effect of higher temperatures on!· arizonensis. Adult bruchid beetles show a significant positive relationship of metabolic rate with body weight (Fig. 4-4). The cost of living forM. protractus again falls below the regression line, while the per beetle oxygen consumption of ~· amicus is much greater than expected. These metabolic rate curves for adults are not related to either body weight or abundance. M. amicus and N. arizonensis have a similar body size but are both larger than significantly larger than~· A· prosopis and all are protractus. (Tables 1, 5). 125 8 0 6 w f<( a:: 4 u ...J 0 co ~ w ~2 20 30 40 50 TEMPERATURE (°C l Fig. 4-3. Metabolic rate -temperature relationships for adults of the mesquite seed beetle guild. All species show a significant increase in oxygen consumption with temperature to 40 or 45°C. There are three distinct groups based on the slopes of the increasing portions of the curves. All slopes are greater than zero (both t and F statistics) and are ranked in the following manner; M. amicus (MA) = f1. protractus (MP)< fl. prosopis (AP)< ~· arizonensis (NA). 126 80 w I- < c: ~ ....J 40 0 CD ~ w ~ 20 30 TEMPERATURE 40 50 ( °C) Fig. 4-4. Metabolic rate - temperature relationships for larvae of the mesquite seed beetle guild. All species show a significant (t and F; P 0.05) increase in oxygen consumption with temperature to 35 or 40°C. The slopes of the increasing portions of the curves are ranked in the following order (95% confidence intervals): ~· prosopis (0.13-1.31) = ~· arizonensis (0.44-1.18) < M. amicus (1.02-2.76). 127 = Y 2.2 7 X + 2.1 8 r2 = 0.698 16 MA NA 12 w ~ <( 0:: lAP j/ u _J 0 ~MA-C SG9 I- ccf 8 co ~ SP¢ w ~ zs 4 ~ I SL ~AP tMP SS? I 2 DRY 4 6 WEIGHT (mgl Fig. 4-5. Relationship of metabolic rate at 30°C with dry weight for 11 species of Bruchidae. Of the four species examined in this study, ~· protractus (MP) falls significantly below the line, while~· amicus (MA) falls significantly above the regression line. Plot is of means ± std. error. The regression is based on data from Kistler (1982), the present study, and from unpublished data. (AP)-~. prosopis; (NA)-R. arizonensis; (CC)-Callosobruchus chinensis; (MA-C)-M. amicus in seeds of Cercidium floridum; (SG)-Stator generalis; (SP)-~. pru1n1nus; (SS)-~. sordidus; (ZS)-Zabrotes subfasciatus. 128 The larvae of the three species examined also show significant increases in metabolic rate with temperature (Fig. 4-5}. The rates of increase again differ with species and fall into two groups. larvae of M. amicus are affected by temperature to a greater extent than the other two species. larvae of M. amicus also have the highest metabolic rate at almost all temperatures. N. arizonensis larvae have the lowest metabolic rate at all temperatures, while A. prosopis is intermediate. larval metabolic rates are also unrelated to adult body size, abundance, or developmental rates, and thus must be related to the cost of resource utilization, the cost of development, or a cost of differing energy utilization and storage strategies. Three measures of reproductive capabilities clearly show that~· amicus has a potential for producing far more eggs than either of the other two species at all temperatures (Fig. 4-6}. This species also shows the greatest variation with temperature. ~· prosopis and N. arizonensis have very similar reproductive capabilities, which are influenced very little by temperature. This lack of an effect of temperature on fecundity is unusual for bruchids, which usually show a curve more similar to that of M. amicus (Kistler 1982, Howe and Curie 1964}. The greatest effect of temperature. on fecundity appears to be an increase in the pre-reproductive period as temperatures decrease. effect is most pronounced in M. amicus and~- This arizonensis, but is of little consequence to A. prosopis (Figs. 6a, 8). Fig. 4-6. A). Curves of mean fecundity for weeks 1-3. Both 111. amicus and N. ari zonensi s show a significant increase in the number of eg·gs laid-as temperature increases (Mean± Standard Error). Much of this increase is due to a decrease in the pre-reproductive period, with increasing temperature. This effect is absent in A. roso is, which shows no significant change with temperature (F(3,-12 = 2.53; P>O.l). B). The maximum number of eggs produced ina single week by each species. C). The total number of eggs laid per lifetime by an average female. Both total and maximum fecundities of~· prosopis and~· arizonensis show no change with temperature, except N. arizonensis shows a significant decrease in total fecundity at 35°C. All three measures show that the fecundity of 1~. amicus is strongly reduced by low temperatures. - 130 ~t~ .. so ......"' 60 ~ ... a: Q. 40 /1----__1" 6 ? Ap I 20 ~120 25 i- 35 30 -f----~ Ma ---aNa ,_ _ _ ]lAp ~~-· 300 240 I ...J ~ 0 >- 120 I ----f~ Ap 1 t-----9~?< 60 ¢ Na I 20 25 30 TEMPERATURE I'Cl 35 131 180 140 <f) >- 100 <.( 0 >- I- > w ~ z 60 0 .....J 0 ¢ ~ ----~ 20 20 25 TEMPERATURE 30 (0 35 () Fig. 4-7. Longevity - temperature relationships for the adult bruchids. The open symbols represent mean values for individuals of all three species that mated and laid eggs. M. amicus often do not lay eggs in the laboratory and their lifespan is increased when this occu.rs (closed triangles). The data points are mean values. Representative error bars are also shown (± 1 std. error). 132 Ap 50 0 20 c 25 <>30 A35 30 10 Na 50 >- 5z 30 ~ v ....... 10 '140 c ·~ 100 GO 20 Ma c \\ __ -o ___ 2 --·-- '·o <>~<>-o --o... ,o\~----o' --- 3 4 5 6 ' 7 8 9 WEEKS Fig. 4-8. Weekly fecundity per lifetime at temperatures from 20°C to 35°C for~- prosopis (Ap), ~- amicus (Ma), and~- arizonensis (Na). Low fecundity during week one represents the effect of temperature on the pre-reproductive period. This was most pronounced in M. amicus at all temperatures, but was totally absent from N. arizonens1s and ~- prosopis at higher temperatures. 133 Longevity of adult beetles increased similarly with decreasing temperature in all three species (Fig. 4-7). ~- Females in general lived longer than males. prosopis lived longer than the other species at most temperatures. N. arizonensis seems again to be adversely affected at higher temperatures. Approximately 15 pairs of~· amicus failed to produce eggs and had a significantly longer life span at all temperatures than those pairs that produced offspring. Increased lifespan at lower temperatures counterbalanced any decrease in number of eggs laid per unit time resulting in equivalent total reproductive output over all temperatures (Fig. 4-8). Developmental rate curves were significantly different for all three species, but all showed a similar pattern of a decrease in developmental rate with decreasing temperature (Fig. 4-9). 0 The linearity of these curves below 30 C allowed an accurate determination of the developmental thresholds (Table 4-4). The thermal constant shown in Table 4-4, is the amount of heat required over time for an insect to complete its development (Messenger 1970). arizonensis requires the most heat, while~- N. prosopis 0 requires the least at temperatures greater than 20 C. Larval survivorship appears to be high at temperatures 0 greater than 25 C. However N. arizonensis and~· prosopis have a very rapid rise in mortality as temperatures drop 0 below 25 C (Fig. 4-10) and again !· arizonensis is the most negatively affected at higher temperatures. 134 4 160 o Ap c:. Ma o Na 0 fT1 < fT1 r (\J 3 0 0 iJ $: z \ ~ \ w 0 fT1 \ X r \ f<( 0:: 120 \ -i \ 2 80 \ $: fT1 .....J ~ 0 z w )> -< :E (j') Q.. 0 _j w a 40 "> w 0 0 20 25 TEMPERATURE 30 (° 35 Cl Fig. 4-9. Developmental rates and times of the egg and larvalpupal stages at the experimental temperatures. The developmental rate of M. amicus was most affected by higher temperatures, while ~- prosopis exhibited the most rapid decrease in developmental rate with decreasing temperature. The standard error of the mean for each value plotted is in all cases less than the size of the symbol depicting that mean. 135 Table 4-4. Temperature constants for bruchids that attack seeds of Prosopis velutina. ESTIMATED DEVELOPMENTAL THRESHOLD (°C)a THERMAL CONSTANT Algarobius prosopis 15.1 698 Mimosestes amicus 12.9 742 Neltumius arizonensis 14.9 820 SPECIES (dd/50)b acaculated by extending the lines in Fig. 4-9 to the abscissa. bcalculated from the mean of the developmental times at 25, 30, and 35°C. 136 1.0 6Ma oNa a.. I (f) 23 0.5 > > 0::: :::::) (f) 0 20 25 TEMPERATURE 30 (° 35 Cl Fig. 4-10. Relative survivorship of larvae at the experimental temperatures. 137 The adult body weights of these four species were different (Table 4-5). The proportion of total weight that was water ranged from a low of 39.1% in M. amicus to about 43% in N. arizonensis and~· prosopis. These values are lower than those reported for CallosobruchHs analis and lower than water content values for many insects (Wightman 1978a). Similarly there were differences in weights of eggs produced by these species. Neltumius arizonensis produces an egg that is significantly larger than the other two species examined, although the water content of the eggs of all three species was around 50%, a value very similar to that found for C. analis (Wightman 1978a) (Table 4-6, Fig. 4-11). The biomass of eggs produced by each species accounted for from 30% to 68% of the total initial adult biomass. Wightman found that egg biomass accounted for only about 10% of initial adult body weight in unfed C. analis. Therefore, in beetles fed on only a sucrose solution, a much greater proportion of initial energy and materials' was expended in egg production. DISCUSSION Previous studies on physiological ecology of the Bruchidae have examined mainly ovarian production, realized fecundity and development of economic species. In most of these studies, the beetles have been dented access to food Table 4-5. Adult weights and percent water for the four members of the mesquite bruchid guild. The regression coefficients for the relationshlp between wet and dry weights are given. mean+SD mean+SD Algarobius prosopis mean+SD mea 6 .06+1. 76* 3. 46+1.04* 43.20+2.46 REGRESSION COEFFICIENTS wet ::: B dry + B0 1 R2 B1 .!_ SE s0 .!_ SE 1.68+0.037 0. 236+0 .132 0.985 Mimosestes amicus 8.07+2.81 4.95+1.80 39 .10+2. 31 * 1.56+0.022* Neltumius arizonensis 8.04+1.60 4.82+0.90. 42. 57+1. 92 1.75+0.060 -0.029+0.294 Mimosestes erotractus - 2.92+0.18* 12.42 13.90 31.64 .001 .001 .001 .05 .01 SPECIES AN OVA F(2 ,97} p Scheffe (P:::0.05} WET WEIGHT *Apd1acNa DRY· WEIGHT *Mp:::Ap Ma:::Na PERCENT WATER 0. 358+0 .115* 0.994 0.963 *Ma<Ap:::Na ....... w (X) Table 4-6. Egg weights and percent water for the members of the mesqu1te bruchia guild. SPECIES DRY WEIGHT PERCENT WATER mean+sd .0217+.00178 .01052 . 513+ .0398 .304 1.12 Mimosestes amicus {N-40) .0224+.00195 .0118 .471+.0460 .679 3.02 Neltumius arizonensis (N=50) .0502+.00123* .02615 .478+.0127 .472 2.09 451.7 - 1.72 Algarobi us {N-40) prosopi~ -- ~-- ANOVA F{2,10) p * .001 - RAnol WATER2 USED (mg) WET WEIGHT mean+sd N.S. 1Ratio of mean total lifetime egg weight (dry)/mean dry body weight. 2The amount of water (weight) expended in egg production for each species. ....... w 1.0 15 .. o 6 0 Ap Ma Na 6 6 6 'a ooo {)) Do 00 E 9 cfbo6DA a:aoa II o <..? o~ w 3: 0 0 0 1- 0 w 3: 6 0 3 ~$ DDAA 6 6 A A Ai:Z> 6 A A oX~ ~OA 0 0 0 A 0 3 DRY 5 7 9 WEIGHT (mgl Fig. 4-11. Relation between wet weight and dry weight of adults. The slope of the relationship forM. amicus is significantly less than that for the other two species, indicating that this species has a lower water content than the other two species. Regression equations and statistics are given in Table 4-5. ....... """ 0 141 or water, and only one species has been examined. The basis for such studies rests on the assumption that when adult beetles emerge from their host seeds, they contain sufficient potential energy and nutrients to initiate the next generation. Even though this assumption has a limited truth in the real world, some significant results have emerged from such studies. Ripe pods or seeds stimulate oogenesis in females and receptivity to mating attempts by males, depending on whether eggs are laid on pods or seeds in nature (Pierre 1980, Sandner and Pankanin 1973, Pimbert and Pierre 1983). There is an unclear interplay between reproductive costs and longevity (Bushnell and Boughton 1940, Gokhale and Srivastava 1975, Huignard and Biemont 1978, Leroi 1980). Temperature mainly affects longevity- of adults and this effect varies between species (Sharma et al. 1979, Utida 1971), but may also affect both male and female reproductive capacities (Huignard and Biemont 1974, Hamed 1981). More recent studies have shown that food may be very important to female bruchids, affecting both longevity and reproductive capabilities (Leroi 1978, Pesho and VanHouten 1982). Male copulatory secretions may also play a role in female nutrition (Huignard 1983). Studies involving bruchids fed with mixtures of pollen, honey and water have demonstrated that there is no significant relationship between adult longevity and the number of offspring produced (Leroi 1978). 142 This study is an attempt to examine the comparative physiological ecology of a single guild of bruchid beetles that attack the same host seeds. Adults were provided unlimited access to food to simulate field nutritional conditions where access to pollen and nectar may be unlimited. In the following discussion I shall discuss the responses of each species separately and then show how these different responses may affect the guild structure as a whole. Algarobius prosopis is the most abundant member of the mesquite seed beetle guild, destroying over 90% of all attacked seeds (Swier 1974, Conway 1980, Table 4-1). There are four outstanding features in the physiological capabilities of this species. Adults live longer than the other species at all temperatures. Reproduction is more independent of temperature than all other species. The metabolic rates of larvae are least affected by temperature and their developmental rate is most rapid at the temperatures usually experienced in the field. These factors undoubtedly play an important role in the successful strategy ad~ptive. of~· prosopis, while other factors seem to be less Adult metabolic rate is largely dependent on external temperature, but this limitation may be circumvented by diurnal activity patterns. Adult fecundity is very low and in two out of three of the measures of fecundity it is lower than all the other species. Females expend less of their initial biomass in egg production than 143 the other species. Larvae appear to be intermediate in their efficiency of utilization of host seeds, based on larval metabolic rates. The larvae are more efficient than ~. amicus but less so than !· ari.zonensis. These apparently negative factors may be less important since fecundity is often unrelated to success (Price 1974), as it is often outweighed by such factors as survival of young and longevity. Also, ~· prosopis is more physiologically efficient in host seed utilization than its closest potential competitor, M. amicus. Mimosestes amicus is the only member of the guild that is not a specialist on mesquite seeds and yet it is the second most abundant species. The most unique feature of this species was its tremendous reproductive capacity. It is capable of producing and laying three times as many eggs as the other two species. Adults are able to regulate their metabolism at a fairly constant level regardless of external temperatures. This may be important for a generalist species attacking hosts with widely varied phenologies, spanning a wide temporal range throughout the growing season in a desert habitat. Furthermore, adults in the absence of appropriate hosts may live for extended periods of time (>160 days in this study) irrespective of external temperatures. This capability was not evident in any of the other species and may again be related to their wide use of resources with different phenologies. M. amicus larvae develop rapidly (intermediate) but were more successful at 144 developing at all temperatures than the other two species as evidenced by both their low developmental threshold and their low larval mortality. In contrast to these successful adaptations are several that appear to have a negative impact. Adults have a very low water content, but expend on the average 3.02 mg of water (97% of initial water content) and 68% of initial biomass in egg production. Associated with the longer preovipositional period (Fig. 4-8) and the fact that oviposition rarely occurs in the absence of food, these three factors point to an extreme dependence on external sources of food and water. In contrast to the adults, larvae are more sensitive to temperature. Larvae are also the least efficient at use of P. velutina as a resource, based on their significantly higher metabolic rate, which indicates a very high relative cost of total development. M. amicus thus appears to have a different set of environmental limitations than~· prosopis, mainly based on a high apparent metabolic and nutrient cost of resource utilization by both adults and larvae, but also appears to be more adapted in reprodu~tive capabilities, survival and development of larvae. Neltumius arizonensis is one of two rare species that are members of the guild. The only striking feature apparent from this study is the very low metabolic rate of its larval stage. Part of this low respiration rate might be due to the slower developmental rate. However, when this 145 is taken into account development still takes considerably less total energy than that of ~· amicus or A. prosopis. The metabolic rate of the larval stage is also not greatly affected by temperature. Thus, I conclude that N. arizonensis is the most efficient at feeding in seeds of P. velutina. Adults and larvae, however, are more temperature dependent than the other species. Temperature has a more consistently negative effect on fecundity in this species. Developmental rate is significantly slower at all temperatures and both adults and larvae are more negatively affected by both high and low temperatures. N. arizonensis thus appears to be more limited by abiotic factors than either ~· amicus or~· prosopis. Mimosestes protractus is the least abundant member of the guild in north-central Arizona, although it may be more abundant (but still minor) further south at lower elevations (Conway 1980). Because it attacks only green pods and is most likely univoltine, very little data are available. has the lowest adult metabolic rate. It This may be due to a decrease in metabolism to a diapause-like state, in the absence of appropriate hosts (i.e., green pods). Natural selection should favor optimal adaptation to environmental and host characteristics. Developmental rate should be maximized to decrease exposure to the environment, parasitoids, predators and competitors (Spence et al. 1980). The cost of development should however, be minimized, as should the cost of response to environmental variation. 146 Production of eggs need not be maximized, but the intrinsic rate of increase, r, should be maximized. The environment (the seed) is identical for the three most abundant species that attack mature seeds and pods. This study, however, shows that beetles in the mesquite seed beetle guild possess no single optimal solution to environmental and host adaptation, even though this might be expected. As a generalist, M. amicus appears to have sacrificed some resource adaptation for a more maximal environmental adaptation. Maximal reproductive output allows it to utilize many hosts and although the generalist larvae are less efficient, their overall success is high. undoubtedly limits the abundance of~· This amicus on any one resource but its overall abundance in the environment across all of its hosts and across time may be considerably higher. Cercidium floridum Bentham is a more preferred host forM. amicus. The metabolic cost of development is much less on seeds of this plant and~· amicus is the most abundant bruchid on this host, indicating that larval utilization efficiency might be important in determining abundance in the bruchid guild (Johnson and Kistler 1985). Mimosestes protractus has become an extreme resource specialist. It has decreased its metabolic costs and body size, and specialized its larval morphology so that it may efficiently utilize a smaller (i.e., less well developed seed) but less utilized resource. (A. prosopis is the only other species that purportedly can attack green pods 147 (Kingsolver et al. 1977} but Fig. 4-1 clearly indicates that more mature green pods are preferred}. However, this strategy limits it to one or at most two generations per year and thus although it may be successful (i.e., have relatively constant populations} it will be less abundant than the other species. Although the cost of development appears to be lowest for N. arizonensis in seeds of mesquite, it appears to be the least adapted to the extreme environmental variation that it must face in this desert ecosystem. Adults and larval stages both are more adversely affected by high temperatures (e.g., decreased larval survivorship, decreased developmental rate, decreased longevity, decreased fecundity, and increased metftbolic rate at temperatures 0 greater than 30 C). These physiological limitations may be the reasons that its population peak occurs in Octob~r through December, when high temperatures are not as extreme. In support of this temperature limitation hypothesis is the absence of this species from site 5 in 1982, where pods were produced during July and were mostly gone by mid-August. All other species were abundant. Also this species is often absent from samples taken from more southerly populations (Conway 1980, chapter 5}. Late in the summer when this species is most active, the resource (number of pods) is decreasing as pods fall from the tree (N. arizonensis and M. amicus do not oviposit on pods after they have fallen to the ground). Thus the decreased resource availability and 148 decreased period of potential resource use may result in the rarity of N. arizonensis in the mesquite seed beetle guild. The large eggs produced by!· arizonensis may also contribute to its relatively low .abundance and to its shift to oviposition in late summer. eggs, of ~· Mitchell (1977) found that amicus, which were laid under other eggs, and of Stator limbatus, which were laid inside a seed pod of Cercidium floridum, had only a 15 to 20% mortality rate due to heat and desiccation, while eggs exposed on the pod surface suffered a much higher temperature related mortality (23 to 50%). Eggs of N. arizonensis are more than twice as large as the eggs of any of the other species and because of their larger overall surface area, heat o~ desiccation related death of the eggs might be even greater than the high levels found by Mitchell. By shifting its resource utilization to late summer it could avoid temperature extremes that would increase mortality of adults, larvae and eggs. The more rapid developmental rate, longer adult life, relative independence of temperature effects on oviposition and on larval metabolic rates, and smaller adult body size all indicate that~· prosopis is relatively more adapted ~o utilization of mesquite as a resource, as well as being more adapted to the harsh diurnal temperature fluctuations and seasonal extremes faced by these bruchids. This species seems to be especially adapted to higher temperatures (35°C) common during the peak of the pod population in July and 149 August. However, just these physiological factors alone do not make a convincing picture as to successful. why~· prosopis is so The major difference between this species and the other three is their distinctly different oviposition behavior. Oviposition in crevices on the pods, and emergence holes of other bruchids significantly decreases temperature related egg mortality (Mitchell (1977) in other bruchid species and so is likely to reduce egg mortality in ~· prosopis also. ~- prosopis also inserts eggs into the matrix structure of the pod wall, which could reduce abiotically induced mortality even more. Factors other than temperature-related phenomena may also influence the structure of this guild of bruchids. There is a large amount of spatial and temporal variability in mesquite seed numbers and quality (chapters 2, 3). This variation is equal for all species and so should not cause the observed differences in relative abundance and timing of the bruchids, but it may contribute to a maintenance of rare species (e.g., the absence of the two rare species from samples in 1982) as rare species. Parasitoids of the larvae attack all four species but may preferentially attack the larger larvae of M. amicus and~· arizonensis, while they may be relatively less able to locate the smaller larvae of ~- prosopis (chapter 5). Simil~rly, the larger eggs of N. arizonensis may be more apparent to parasitoids that attack the eggs, as well as to other egg predators, whereas the "secretive" oviposition strategy of~- prosopis 150 significantly decreases egg parasitism relative to the exposed eggs of the other species (Bridwell 1918, chapter 5)• Abundance must be a function of resource availability and predictability, and fecundity-mortality events, influenced to some extent by larval developmental rates. As was mentioned above, resource availability and predictability should be equal for all species in the mesquite guild and so should not play an important role in the species abundances (except as morphological and physiological parameters restrict them to smaller subsets of the total resource pool). Fecundity of the species in the guild is independent of the observed abundances (i.e., the most fecund is not the most abundant). Population growth rates and abundances thus must be due to mortality events (real or potential) due to predation or abiotic limitations, such as differential tolerances to temperature and moisture stresses imposed on the populations by the harsh and unpredictable desert environment. This study was designed to address the abiotic factors that might limit these populations, while other papers deal with resource variation and parasitoids and their effects on the bruchids (chapters 3, 5). Temperature was chosen as the variable most likely to limit these popul~tions since moisture stress should only occur at the egg and adult stages, because the larvae survive on seed water content and metabolic water and are surrounded by an impermeable seed coat during development. 151 The data indicate that life history parameters (fecundity, longevity, survivorship) of~· prosopis are least affected by high temperatures such as those that occur during the peak of pod production. Associated with this resistance to high temperatures is a significantly greater 0 developmental rate at all temperatures greater than 25 C. !· arizonensis is negatively affected by high temperatures more than any of the other two more abundant species (large egg size, survivorship, growth rate, fecundity, longevity, adult metabolic rate) and develops more slowly at all temperatures. M. amicus lies between these two extremes, showing negative effects of temperature on larval metabolic rates and fecundity and an intermediate developmental rate. All of these species are thus affected by temperature and, the degree of adaptation to high temperatures and to rapid temperature changes seems to be associated with the abundance of the species. It is not clear from these data that temperature is the main factor limiting overall abundance of the species. Studies need to be done to examine abiotically caused egg mortalities in the different species to complete this picture. A second purpose of this study was to see if temperature limitation might be able to explain the temporal distribution of the species abundance curves (Fig. 4-1), which had previously been attributed to competitive interactions. M. protractus utilizes only green pods as a resource and does not attack the other two pod stages. This 152 factor alone explains its abundance peak being shifted to the left of all the other species. During this early green pod stage, it may constitute up to 30% of the total bruchid population, demonstrating its effective utilization of an under-utilized resource, while at the same time allowing it to attack before parasitoids of its eggs and larvae have a chance to build up their populations. Green pods are also a much more abundant and predictable resource but pod abortion increases the chances of a wasted oviposition at these early stages (chapter 2). Since internal temperatures of green pods are equivalent to ambient temperatures, temperature stress on these pods at this hottest time of the year will probably not be any greater than that experienced by the other species in dry pods later in the summer. The peak of the populations of~· prosopis and M. amicus occur during the peak of resource abundance. The relative temperature independence of these two species allows them to utilize this resource peak. The low total abundance of bruchids even during periods of low resource abundance (pods and seeds), apparently allows both species to share this temporal niche with little or no apparent selection for competitive divergence. Since~· amicus is a generalist with other potential host species, switching to mesquite as a host would be most beneficial during the resource peak. Thus, its timing may be simply a result of its generalist strategy. Examination of the population dynamics and phenology of M. amicus on its alternattve hosts would 153 provide insight into its overall strategy and population abundance. Lastly, the population peak of N. arizonensis appears to be shifted toward the cooler months of the summer (and early spring). This shift ~ppears to be caused largely by its inability to tolerate high temperatures which negatively affect egg survival and other life history parameters. At the same time, this shift may reduce the probability of potential competitive interactions between larvae of this species and the two more abundant species. The inability to tolerate high temperatures may limit the numbers of this species due to decreased resource abundance, a limitation of population growth rates by lower temperatures, and a build up of parasitoid populations by this time in the season. be an optimal strategy for This definitely does not appear to ~· arizonensis. Its continued existence in the mesquite bruchid guild argues strongly against a competitive explanation for the temporal distributions and abundances within the guild. Temperature related phenomena can thus strongly influence species abundances and temporal distributions in this guild of bruchid beetles. It may also maintain populations of all of these species below levels where interspecies interactions and competition might occur. 154 LITERATURE CITED Bridwell, J. C. 1918. Notes on the Bruchidae and their parasitoids in the Hawaiian Islands. Entomol. Soc. Proc. Hawaiian 3:465-509~ Bursell, E. 1964. Environmental aspects: 283- 321. In: temperature. pp. M. Rockstein (ed.). Vol. 1, The physiology of Insecta, Academic Press, New York. Bushnell, R. J. and D. C. Boughton. 1940. Longevity and egg production in the common bean weevil, Acanthoscelides obtectus. Ann. Entomol. Soc. Amer. Clarke, K. U. 1967. In: 33:361-370. Insects and temperature. pp. 293-352. A. H. Rose, Thermobiology, Academic Press, New York. Conway, R. 1980. A comparative study of the bruchid-parasitoid complexes found in some Arizona legumes. Unpub. M.S. Thesis, Northern Arizona University, 99pp. Doyen, J.T. and C.N. Slobodchikoff. 1984. Evolution of microgeographic races without isolation in a coastal dune beetle. J. Biogeog. 11:13-25. Fujii, K. 1967. Studies on interspecies competition between the Azuki bean weevil, Callosobruchus chinensis , and the Southern cowpea weevil, C. maculatus. II. different environmental conditions. 9:192-200. Competition under Res. Popul. Ecol. 155 Gokhale, V. G. and B. K. Srivastava. 1975. Ovipositional behavior of Callosobruchus maculatus (Fabricius) (Coleoptera:Bruchidae). I. Distribution of eggs and relative ovipositional preference on several leguminous seeds. Indian J. Entomol. 37:122-128. Hamed, M.S. 1981. Effect of heat on the fecundity of the bean weevil Acanthoscelides obtectus (Coleoptera, Bruchidae). Z. Angew. Entomol. 91:368-374. Howe, R. W. and J. E. Currie. 1964. Some laboratory observations on the rates of development, mortality and oviposition of several species of Bruchidae breeding in stored pulses. Bull. Entomol. Res. 55:437-477. Huignard, J. 1983. Transfer and fate of male secretions deposited in the spermatorphore of females of Acanthoscelides obtectus Say (Coleoptera, Bruchidae). J. Insect Physiol. 29:55-63. Huignard, J. and J. c. Biemont. 1974. Effect of an increase of temperature on the male reproductive capacity of Acanthoscelides obtectus Say (Coleoptera, Bruchidae). Ann. Zo o 1 • Ec o 1 • .A n i m• 6 : 5 6 1- 5 7 4 . Huignard, J. and J. c. Biemont. 1978. Comparison of four populations of Acanthoscelides obtectus (Coleoptera:Bruchidae) from different Colombian ecosystems. Oecologia 35:307-318. 156 Johnson, C. D. 1978. Ecology of Neltumius texanus (Coleoptera:Bruchidae) in seeds of Condalia (Rhamnaceae). J. Kans. Entomol. Soc. 51:432-440. Johnson, C. D. 1981a. Seed beetle host specificity and the systematics of the leguminosae. pp. 995-1027, In: R. M. Polhill and P. H. Raven (eds.). Advances in legume Systematics, Royal Botanic Gardens, Kew. Johnson, C. D. 1981b. Interactions between bruchid (Coleoptera) feeding guilds and behavioral patterns of the pods of the leguminosae. Environ. Entomol. 10:249-253. Johnson, C.D. and R.A. Kistler. 1985. Nutritional ecology of bruchid beetles. In: F. Slansky Jr. and J.G. Rodriguez (eds.). Nutritional ecology of insects, mites and spiders, John Wiley and Sons, New York, submitted. Keister, M. and J. Buck. 1974.· Respiration: some exogenous and endogenous effects and rate of respiration. pp. 469-509. In: M. Rockstein (ed. ). Physiology of Insecta, Vol. 6, Academic Press, New York. Kingsolver, J. M. 1964. The genus Neltumius (Coleoptera:Bruchidae. Coleopt. Bull. 18:105-111. Kingsolver, J. M. and C. D. Johnson. 1978. Systematics of the genus Mimosestes (Coleoptera:Bruchidae). Agric. Tech. Bull. 1590, 106pp. u.s. Dept. 157 Kingsolver, J. M., C. D. Johnson, S. R. Swier, and A. Teran. 1977. Prosopis fruits as a resource of invertebrates. pp. 108-122. In: B. B. Simpson (ed. ). Mesquite: its biology in two desert shrub ecosystems. Dowden, Hutchinson and Ross, Stroudsburg, Pennsylvania. Kistler, R. A. 1982. Effects of temperature on six species of seed beetles (Coleoptera:Bruchidae): an ecological perspective. Ann. Entomol. Soc. Amer. 75:266-271. Kunhikannan, K. 1923. The function of the prothoracic plate in Mylabrid (Bruchid) larvae, (A study in adaptation). Mysore State Dept. Agr., Ent. Ser. Bull. 7, 47pp. Lawton, J.H. and D. R. Strong. 1981. competition in folivorous insects. Community patterns and Am. Nat. 118:317-338. Leroi, B. 1978. Feeding of adults of Acanthoscelides obtectus Say (Coleoptera:Bruchidae). Influence upon the longevity and ovarian production of virgin individuals. Ann. Zool. Ecol. Anim. 10:559-568. Leroi, B. 1980. Regulation of egg production in Acanthoscelides obtectus (Coleoptera:Bruchidae): The change in stimulating effect of grain on females of different ages. Entomol. Exp. Appl. 28:132-144. May, M. L. 1979. Insect thermoregulation. Annu. Rev. Entomol. 24:313-349. 158 Messenger, P. S. 1970. Bioclimatic inputs to biological control and pest management programs. pp. 84-99. In: R. L. Rabb and E. E. Guthrie (eds. ). Concepts of pest management. North Carolina State University Press, Raleigh, North Carolina. Mitchell, R. 1977. Bruchid beetles and seed packaging by palo verde. Ecology 58:644-651. Mutchmor, J. A. 1967. Temperature adaptation in insects. pp 165-176. In: C.L. Prosser (ed. ). Molecular mechanisms of temperature adaptation. Pub. No. 84. AAAS, Washington, D. C. Park, T. 1954. competition. Experimental studies of interspecific II. Temperature, humidity and competition in two species of Tribolium. Physiol. Zool. 27:177-231. Pesho, G. R. and R. J. Van Houten. 1982. Pollen and sexual maturation of the pea weevil. Ann. Entomol. Soc. Amer. 439-443. Pfaffenberger, G. S. and C. D. Johnson. 1976. Biosystematics of the first-stage larvae of some North American Bruchidae (Coleoptera). U.S. Dept. Agric. Tech. Bull. 1525. 75 pp. Pierre, D. 1980. Influence of seeds or ripe pods of Phaseolus vulgaris on the reproductive activity of Zabrotes subfasciatus (Coleoptera: Bruchidae). C. R. Hebd. Seances Acad. Sci. Ser. D. Sci. Nat. 290:1007-1010. 159 Pimbert, M. P. and D. Pierre. 1983. Ecophysiological aspects of bruchid reproduction. I. The influence of pod maturity and seeds of Phaseolus vulgaris and the influence of insemination on the reproductive activity of Zabrotes subfasciatus. Ecol. Entomol. 8:87-94. Price, P.W. 1974. Strategies for egg production. Evolution 28:76-84. Rathcke, B. J. 1976. Competition and coexistence within a guild of herbivorous insects. Ecology 57:76-87. Sandner, H. and M. Pankanin. 1973. Effect of the presence of food on egg-laying by Acanthoscelides obtectus Say (Coleoptera,Bruchidae). Pol. Pismo. Entomol. 43:811-817. Sharma, S. P., S. Rattan, and G. Sharma. 1979. Temperature dependent longevity of Zabrotes subfasciatus (Coleoptera: Bruchidae). Camp. Physiol. Ecol. 4:229-231. Simberloff, D. and E. F. Connor. 1981. Missing species combinations. Am. Nat. 118:215-239. Spence, J. R., D. H. Spence, and G. G. E. Scudder. 1980. The effects of temperature on growth and development of water strider species (Heteroptera:Gerridae) of Central British Columbia and implications for species packing. Zool. 58:1813-1820. Can. J. 160 Swier, S. R. 1974. Comparative seed predation strategies of mesquite bruchids in Arizona, with particular reference to seed height, direction and density. Unpublished M.S. Thesis, Northern Arizona University, Flagstaff, Arizona. 97pp. Taylor, V. A. 1980. Coexistence of two species of Ptinella Motschulsky (Coleoptera:Ptiliidae) and the significance of their adaptation to different temperature ranges. Ecol. Entomol 5:397-411. Utida, S. 1971. Influence of temperature on the number of eggs, mortality, and development of several species of bruchid infesting stored beans. Jap. J. Appl. Entomol. Zool. 15:23-30. Wiens, J. A. 1977. On competition and variable environments. Amer.Sci. 65:590-597. Wightman, J. A. 1978a. The ecology of Callosobruchus analis (Coleoptera:Bruchidae): morphometries and energetics of the immature stages. J. Anim. Ecol. 47:117-129. Wightman, J. A. 1978b. The ecology of Callosobruchus analis (Coleoptera:Bruchidae): energetics and energy reservers of the adults. J. Anim. Ecol. 47:131-142. CHAPTER 5 The Role of the Third Trophic Level in the Mesquite-Bruchid Ecosystem. 161 162 INTRODUCTION Most knowledge of ecological communities is limited to at most two trophic levels, with a striking void of information on the roles played by predators and parasitoids in communities, despite the fact that all three major trophic levels appear to be tightly linked. Because of this paucity of knowledge about the uppermost trophic levels, ecologists have began to examine the role of the third trophic level in the evolution of both organisms and communities (Price et al. 1980). This new emphasis has shown that communities of herbivorous insects may be more limited by natural enemies then by other factors, like competition, that have been thought prominent in the past (Lawton and Strong 1981). Thus, selection for enemy free space (Lawton 1978) may be more prominent than intra-trophic level interactions (Price 1983). This study examined the role of parasitoids in a mesquite-bruchid ecosystem (Leguminosae:Prosopis velutina Wooten, Coleoptera:Bruchidae) in central Arizona. In light of the general lack of knowledge about the significance of parasitoids in insect communities the major question asked in this study was if the community of parasitoids is important enough to exert a selective influence on the seed predator community. A secondary question asked whether or not the parasitoid community exerts a differential influence 163 on the members of the seed-predator community, thus acting as an organizing factor in this community. METHODS The populations of parasitoids were monitored through a three year series of field collections of mesquite pods and laboratory rearings as described in chapter 2. A subsample of these pods were examined immediately upon collection and the number of bruchid eggs present on the external surface of the pods was counted. The number of these eggs that had been parasitized by trichogrammatid egg parasitoids was recorded. To further examine the parasitoid community, field experiments were undertaken in which cages (20cm X 10cm X 10cm) made of 1/4 inch (6.4mm) mesh galvanized hardware cloth were filled with 15 mesquite pods, collected from the population in 1982. These were then hung in a tree which had produced no pods in 1983. Two sets of experiments were carried out, with five replicate cages of each set. The entire set was then replicated in two distinct populations. To examine the egg parasite population, a laboratory culture of Mimosestes amicus (Horn) was allowed to freely oviposit on a large number of pods for a three-day period. These pods were then divided randomly into groups of 15 pods, placed into the cages and hung in trees during August 1983, (tree #4 at site 5 and tree #10 at site 4), with five cages per tree. After 13 days all eggs were counted and 164 classified as dead, hatched, or parasitized. These same cages were used to examine parasitoids of early instar bruchids. After this thirteen-day period in the field, the cages were collected, the pods were placed into jars, and the bruchids and parasitoids were reared as described in chapter 2. The second set of experiments examined the parasitoid community that attacks older instar bruchids, in the same manner as described above. However, the~· amicus larvae were allowed to develop for 21 days prior to placing the pods in cages and hanging them in the experimental trees in the field. These pods were collected 10 days later just prior to emergence of adult bruchids. These experiments thus acted as a bioassay for the parasitoid community attacking the eggs, early instar, and late instar and pupal stages of the bruchid community. The possibility of differential rates of parasitism within the bruchid community was examined in a set of laboratory experiments. Three species of parasitoids were used; egg parasitoids (Trichogrammatidae), Heterospilus prosopidis Viereck (Braconidae) and Eupelmus cyaniceps Ashmead (Eupelmidae). prosopis, ~· amicus, Fifteen pods containing or~· la~vae of A. arizonensis of the appropriate stage {eggs or 20 day old larvae) were placed into jars with 20 pairs of parasitoids. Three replicates were used for larval parasitoids and 12-were used for the egg parasitoid tests. 165 RESULTS AND DISCUSSION The population dynamics of the bruchids and larval parasitoids varied between years as well as within each year (Fig. 5-1). The prominent resuli of these data was that the parasitoid population closely followed the dynamics of the host bruchid populations, but with a slight time lag. This is typical for parasitoid-host populations in general (Hassell 1978) and for bruchid-parasitoid populations (Fujii 1983, Kistler 1979). However, Figure 5-1 underestimates the importance of the parasitoids. Once pods were collected from the field all larvae in the pods were instantaneously removed from further parasitism which probably would still occur in the field. To achieve a more realistic measure of the importance of parasitism (probably still an underestimate), parasite populations were examined in comparison with only the first two weeks of bruchid emergence in 1983 (Fig. 5-2). From these data it was apparent that parasitism ranged up to 50% of the total number of larvae per 30 pod sample. It appeared possible that populations of both egg and larval parasitoids might strongly influence population dynamics of the bruchid guild. This possibility was examined further for the egg parasitoid populations by field counts of actual eggs parasitized in comparison with the total number of eggs per 30 pod sample (Fig. 5-3). Fifty to 100% of all eggs on the external surface of the pods were parasitized and there was a strong 166 0 I 90 I I I 0 I \ I I I I 0 \ i 60 0 1\ vo a: w CD :::0 ::::> 0 I I I I 0 z 30 \J 0 I I . 0 . I I I 0 0 \' I 0 Q I \ ~ 0 1\ 0 ' .0 0 o' ""-. . p I ~• 0 ' I ' I I ' ., ' o"'~ .?-o i:J.-0 '"0 ,' ! I' 0 '' _o ~ l.J.()oU ; ,' \_ O~o~-.-~~Jdl~~-o~,o~/4--+o--r-----+~~a+-'~o~~~o-~o~--~+--+~~-r.~ 9/1 7/1 1980 9/1 1981 1111 9/1 11/1 1982 8/1 10/1 1983 9/12 1984 DATE Fig. 5-1. Population dynamics of the larval parasitoids (squares) and their host bruchids in the mesquite ecosystem (circles) from 1980 to 1984 at site 1. These numbers represent the number of successful emergences from pods maintained for 35 days in the laboratory and are thus a measure more of potential than real population levels. The parasitoid populations closely follow the pattern in the bruchid populations. The bruchid population is highly dependent upon the resource seed dynamics (chapter 2). 0 BRUCHIDS 12 o LARVAL P t::. EGG P 9 1 0:: w6 CD ~ / !::.' :J z 3 ' ~'f ' .......... ' '~::. ..... ""-....._ g/ -~o/~~yo ..... ..... '!::.-- ' ' ----7/30 8;13 22 9/1 13 22 10/3 17 19 8 3 DATE Fig. 5-2. Population dynamics of the bruchids (circles), larval parasitoids (squares), and egg parasitoids (triangles) in the mesquite ecosystem for the 1983 season at site 1. These data are based upon only the first two weeks of insect emergence after the pods were collected. This gives a more accurate estimate of the actual dynamics of these populations in the field than Fig. 5-1. Egg parasitoid populations are high until pods began to fall from the trees, while the larval parasitoids follow the dynamics of their host population more closely. ...... 0'1 '-J 168 linear relationship between the total number of eggs and the number of eggs parasitized. The egg parasites possessed a strong capability to regulate the overall populations of bruchids in the field. Because of the dependency of this study upon laboratory rearing of field samples, it was more difficult to determine the instantaneous importance of larval parasitoids. That larval parasitoids may also strongly limit or regulate bruchid populations was indicated by three lines of evidence. First, the community of parasitoids found in this study was extremely diverse (Table 5-1, Fig. 1-1), indicating a relatively stable resource pool to support these species. Secondly, two factors point toward a relatively high probability of competitive interactions between species of parasitoids, indicating a limiting resource in the second trophic level. are very low. Bruchid populations An examination of Fig. 5-2 indicates a maximum density of only one bruchid larva per every three pods. There was also a definite division of the resource by bruchid instar, with Urisigalphus bruchi specializing on early instars and Heterospilus prosopis specializing on later instars (Fig. 5-4). There was also some circumstantial evidence that some of the smaller species (especially 3 species of Eulophidae) might also specialize on larvae in green pods while all other species prefer bruchids in more mature pods. 169 120 R2 =0. 81 p =.001 • 0 w 80 N I(/) <( a:: ~ 0 .40 z 40 NO. 80 120 EGGS Fig. 5-3. There is a significant linear relationship between the number of bruchid eggs on the external surface of mesquite pods in the field and the number of these eggs that have been parasitized by trichogrammatid egg parasitoids. The regression equation is; Y = 0.619X- 0.9, F(1, 18) = 77.1. 170 Table 5-l. Parasi toi ds of the mes.qui te seed predator gui 1d. MOTH PARASITOIDS Hymenoptera Braconidae Agathis tenuiceps Species A Species B Ichneumonidae Temelucha sp. Diptera Tachinidae Species A BRUCHID PARASITOIDS Egg Parasitoids Hymenoptera Trichogrammatidae Trichogramma spp. ? Larval Parasitoids Hymenoptera Braconidae Bracon therberi phage Apanteles sp. Heterospilus prosopidis Urisigalphus bruchi Eulophidae Horismenus productus Hyssopus evetriae Tetrastichus dologus 7 misc. species ? Eupelmidae Eupelmus cyaniceps Eurytomi dae Eurytoma sp. LARVAL AGE (daysl <13 22-32 CR BC Fig. 5-4. The major larval parasitoids in the system appear to have subdivided their host larval resource by larval size. Urisi al hus bruchi (UB) attacks mainly young larvae, while Heterospilus prosopidis HP attacks mainly older larvae. Two other parasitoids also attack mainly late instars (Eupelmus cyaniceps (EC) and Urytoma sp. (U)). The numbers in the figure refer to the total numbers that were reared from these caged pods at each of two sites (CR = site 5 and BC = site 4). ....... -....J ....... 172 100 0 w N ~ (./) <t: 60 a:: <t: Q.. (./) ~ ~ w ~ 0 20 AP MA NA Fig. 5-5. Differential rates of parasitism of the eggs of three species of bruchids by trichogrammatid egg parasitoids occurred in laboratory tests. The eggs of fl. prosopis (AP) were attacked significantly less often than the eggs of M. amicus (MA) and N. arizonensis (NA) (ANOVA, F= 13.51; df=2-;- 27; P< .001). Vertical bars represent 95% confidence intervals. 173 The third factor that indicated the importance of larval parasitoids was that they appear to be extreme generalists. In the laboratory tests, neither Heterospilus prosopidis nor Eupelmus cyaniceps showed any preference for any bruchid species. This generalist behavior would tend to equalize the populations of the four bruchid species in a density dependent manner. Thus the low numbers of bruchids, the generalist nature of the parasitoids, which is unusual in parasitic Hymenoptera (Price 1980, M. Hetz pers. comm.), and the subdivision of the larval resource among the parasitoid species all indicate that bruchid larvae might be a limiting resource for the parasitoids. These factors also indicate that competitive interactions might occur (exploitation competition) within this very diverse guild of parasitoids that makes up the third trophic level in the mesquite-bruchid ecosystem. Do these parasitoids play any role in the organization of the bruchid community? It is clear from the above data that their impact upon the bruchid populations was quite extensive during the three years of this study. They have a potential to act as regulatory agents upon the bruchid population as a whole, allowing all four species to coexist in the same resource with very little or no interspecies interactions (Chapter 3). They may also act in a differential manner, affecting different bruchid species to different extents. This was supported by data on egg parasitism but not that on larval parasitism. In the 174 laboratory, egg parasitoids were less able to find and parasitize the eggs of ~· prosopis, which are hidden in the mesocarp of the pod or placed in groups in the exit holes of other insects or in other damaged areas on the pods. They are more efficient at parasitizing the eggs of the other species which are glued to the external surface of the pods (Chapter 3, Fig. 5-5, Bridwell 1918). These egg parasitoids may thus play an important role in the organization of the bruchid guild in mesquite, by allowing~· prosopis to be the dominant bruchid in the guild because of its secretive oviposition behavior. Oviposition behavior has been shown to be important in other bruchid populations in desert ecosystems (Mitchell 1977). In conclusion, parasitoids may play a very major role in the bruchid-mesquite ecosystem. These data point toward both organizational and regulatory roles for the parasitoid populations and especially for the population of egg parasitoids. 175 LITERATURE CITED Bridwell, J.C. 1918. Notes on the Bruchidae and their parasitoids in the Hawaiian Islands. Proc. Hawaiian Entomol. Soc. 3:465-509. Fujii, K. 1983. Resource dependent stability in an experimental laboratory resource-herbivore-carnivore system. Res. Popul. Ecol. Suppl. 3:15-26. Hassell, M.P. 1978. The dynamics of arthropod predator-prey systems. Princeton University Press, Princeton. Kistler, R.A. 1979. A simple host-parasitoid system: An examination of factors contributing to stability. Unpub. M.S. Thesis, Purdue University, West Lafayette, Indiana, 108pp. Lawton, J.H. 1978. Host-plant influences on insect diversity: the effects of space and time. Symp. R. Entomol. Soc. London 9:105-125. Lawton, J.H. and D.R. Strong. 1981. Community patterns and competition in folivorous insects. Am. Nat. 118:317-338. Mitchell, R. 1977. Bruchid beetles and seed packaging by Palo Verde. Ecology 58:644-651. 176 Price, P.W. 1983. Hypotheses on organization and evolution in herbivorous insect communities. pp. 559-595, In: R.F. Denno and M.S. McClure (eds.). Variable plants and hervbivores in natural and managed systems, Academic Press, New York. Price, P.W., C.E. Bouton, P. Gross, B.A. McPheron, J.N. Thompson and A.E. Weis. 1980. Interactions among three trophic levels: Influence of plants on interactions between insect herbivores and natural enemies. Annu. Rev. Ecol. Syst. 11:41-65. CHAPTER 6 GENERAL DISCUSSION 177 178 Recent discussion in ecology has re-emphasized that single factor explanations for patterns in nature are highly unlikely. Instead, a multiplicity of factors more than likely leads to adaptation of organisms to their ecological and evolutionary settings. Although such an answer is not extremely pleasant to ecologists whose goal has been to search for pattern in natural systems, the current questioning of long standing ecological paradigms is leading to new approaches to answering ecological questions. The importance of physiological responses to resources and the environment (Mitchell 1983, Kistler 1982), the organization and interaction of communities (Lawton and Strong 1981, Price 1983), the importance of variation within a resource (Whitham 1981, Thompson and Price 1977), the real meaning of generalism versus specialism in ecological communities (Cates 1981), and the role of all three trophic levels in ecological communities (Price et al. 1980), have all been examined with a view towards determining their relative importance in communities of plants and animals and their importance as general factors explaining the patterns we see in natural ecosystems. This research examined a three trophic level desert ecosystem consisting of the seeds of Prosopis velutina, a four species guild of seed predators, and a complex guild of parasitoids of the seed predators. The study specifically addressed the importance of environmental variability on both seed_ production and on the physiology and community 179 organization of the guild of seed predators, the impact that such variability has on the population dynamics and guild structure of the seed predators, and the important roles played by the guild of parasitoids in both limiting the seed predator guild and structuring species abundances within the bruchid guild. This type of intensive study, combining field observations and experiments as well as laboratory experiments, and examination of all three trophic levels should lead ecologists to explanations of natural patterns of community organization and interaction in insect-plant communities. Variability in seed production was very prominent in the six populations of Prosopis velutina examined. Alternate year pod and seed production resulting from an interaction of energy and nutrient limitations and the cost of reproduction, accounted-for a large part of the interpopulation variability. Varying levels of reproductive synchrony within the different populations occurred mainly as a result of the highly variable abiotic environment found in these desert ecosystems and indicated little selection by seed predators for such strategies as synchronous predator satiation. Instead, the high variability of seed production within populations and within individual trees points towards the existence of an energy and nutrient threshold, which must be exceeded by individual trees or tree parts every year in order to reproduce successfully. Above this threshold, individual plants allocate different amounts of 180 energy or nutrients to production of pods and seeds, dependent upon abiotic factors and the recent reproductive history of the individual plant. Since experiments were not used to examine limitations on seed production occuring at the flowering stage, the environmental and energy limitation hypothesis for seed production in mesquite is only one possibility which is most strongly supported by these data. The real reproductive strategy may be a more complex combination of flowering strategies based on male versus female fitness, pollinator interactions, dispersal agent interactions, and environmental and energy limitations. The high level of variation at the seed population level did have significant importance for the upper trophic levels. High variation between populations means that seeds are a very unpredictable resource at the local level. Thus, bruchids were unable to build up high local populations. Similarly, the within-tree and within-pod variation made it difficult for the foraging bruchids to locate an appropriate resource seed in which their offspring could successfully develop. Thus, variability in the plant population may actually act as a defensive strategy against the guild of seed predators. Furthermore, this variability did not seem to have a large negative impact upon the parasitoid populations, prpbably because of the extreme generalist nature of these parasitoids which attack a wide variety of bruchids in other host plants in the ecosystem. 181 The bruchids within the mesquite seed predator guild were also differentially limited by abiotic factors, such as temperature-moisture relations in this harsh, unpredictable, desert ecosystem. The distinctly different adaptations to temperature variation exhibited by the four species of bruchids were strongly related with species abundance and success. Temperatur~ was one important factor in determining community organization within this guild. Parasitoids also acted in a differential manner to aid in structuring the bruchid community and limiting overall populations of the seed predator guild. The dominance of Algarobius prosopis in the guild was mainly a result of successful adaptation to the variable abiotic factors and to parasitism by trichogrammatid egg parasitoids. Vari.abilty in the seed resource, abiotic factors, and parasitoids all acted in concert to maintain populations of bruchids below levels at which they might become important as selec.tive agents on reproductive strategies of mesquite over evolutionary time. The key factor analysis clearly supports the relative unimportance of this entire guild of seed predators. When compared to the other pre-predation ovule and seed mortality factors which affect plant reproductive output, the bruchid guild is the least important mortality factor. There is a very complex community of parasitoids in the mesquite-seed predator system. The complexity of this third trophic level community indicates the importance of this trophic level as a potential plant defense through 182 limitation and/or regulation of the seed predator community. The extreme generality of most of the parasitoids in the guild (most species attack bruchids in at least two other host plants in the Verde Valley) .allows more constant population dynamics at the third trophic level than would be likely for specialists on rare mesquite bruchids. Thus parasitoids may act as a community defense (Attsat and O'Dowd 1976). Within the mesquite bruchid guild, egg parasitoids may act as an organizing factor, allowing A. prosopis to be the most abundant bruchid as a result of the failure of the other species to respond to the extremely high levels of egg parasitism. These egg parasitoids are a good defensive mechanism for mesquite seeds and so factors that select for attack by egg parasitoids, such as pods free of crevices (Janzen 1969), which forces the bruchids to lay their eggs on the exposed surface of the pod, or shelter from desiccation provided by the maintenance of leaves throughout the summer, might be expected in desert trees (Mares et al. 1977). This study was not successful in addressing this question of whether trees attempt to attract and maintain populations of parasitoids as a plant defense, but the possibility remains. Trees would be less likely to select for the presence of larval parasitoids since the seed has been killed by the time the parasitoid has killed the bruchid larvae, but the tree might still select for these parasitoids as a general defense, limiting overall seed destruction by bruchids. 183 This study of a three trophic level ecosystem thus supports idea that there is no single factor structuring intertrophic and intratrophic level interactions and community organization. Instead a complex suite of factors ranging from environmental limitation of all trophic levels to intertrophic level interactions may all be equally important in structuring this desert ecosystem. 184 LITERATURE CITED Atsatt, P.R. and D.J. O'Dowd. 1976. Plant defense guilds. Science 193:24-29. Cates, R.G. 1981. ·Host plant predictability and the feeding patterns of monophagous, oligophagous, and polyphagous insect herbivores. Oecologia 48:319-326. Janzen, D.H. 1969. 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Variable plants and herbivores in natural and managed systems. Academic Press, New York. Thompson, J.N. and P.W. Price. 1977. Plant plasticity, phenology, and herbivore dispersion: wild parsnip and the parsnip webworm. Ecology 58:1112-1119. Whitham, T.G. and C.N. Slobodchikoff. 1981. Evolution by individuals, plant-herbivore interaction and mosaics of genetic variability: the adaptive significance of somatic mutations in plants. Oecologia 49:287-292.