Local adaptation in the armored scale insect Pseudaulacaspis pentagona (Homoptera: Diaspididae).
Phytophagous insects often exhibit patchy distributions both within and among their host plants. One possible explanation for this pattern is genetic variability in resistance to their host plants (Hare and Futuyma 1978, Hare 1980, Moran 1981, Wainhouse and Howell 1983, Whitham 1983, Service 1984, Berenbaum et al. 1986, Karban 1987, Maddox and Root 1987, Simms and Rausher 1987, Fritz 1990, Strauss 1990). Variation in resistance traits among host plants may promote genetic diversification in their herbivores (Mitter and Futuyma 1983, Futuyma and Peterson 1985).
The likelihood for genetic polymorphisms in herbivores is increased when herbivores select and reproduce on the host plant species on which survival is highest, and mate assortatively (Levene 1953, Maynard Smith 1966, 1970, Dickinson and Antonovics 1973, Felsenstein 1981, Bush and Diehl 1982). However, the evolution of genetic polymorphisms in mobile herbivores may be constrained due to the unlikely occurrence of linkage disequilibria between loci that govern host location and assortative mating and those that provide for physiological adaptation (Mitter and Futuyma 1983, Futuyma and Peterson 1985). Host-associated polymorphisms may be more likely to arise when gene flow is restricted between herbivore populations (Mitter and Futuyma 1983, Futuyma and Peterson 1985). For example, low mobility and phenological differences between populations can encourage genetic divergence among herbivore populations (Sturgeon and Mitton 1986, Smith 1988, Karban 1989).
Scale insects (Homoptera: Coccoidea) may be predisposed to genetic differentiation over small spatial scales due to their sedentary nature and preference for long-lived host plants (Miller and Kosztarab 1979). Several features of their biology contribute to possible restricted gene flow between populations. These features include: (1) the low mobility of adult females, with feeding and oviposition restricted largely to their natal tree (Miller and Kosztarab 1979); (2) the relative immobility of first-instar crawlers (dispersal stage), which disperse inefficiently within and between trees (e.g., Beardsley and Gonzalez 1975, McClure 1977a, Stephens and Aylor 1978); and (3) the tendency for winged males to mate with nearby females (e.g., Tashiro and Moffitt 1968, Alstad et al. 1980, Hanks and Denno 1993a).
Edmunds and Alstad (1978) suggested that populations of the armored scale insect Nuculaspis californica Coleman were adapted to the defensive properties of individual pine trees and comprised different demes. Furthermore, local adaptation to a particular host may contribute to the contagious distribution of scales within stands of pine trees by impeding the colonization of neighboring trees of differing genotype (Edmunds and Alstad 1978, Alstad and Edmunds 1983).
Edmunds and Alstad (1978) tested for local ("demic") adaptation to individual trees by transferring N. californica from donor trees (1) to receptor trees of presumably different genotype (between-tree transfers) and (2) back to the same donor tree (within-tree transfers). They predicted and found higher scale performance for within-tree transfers than between-tree transfers and concluded that scale populations were better adapted to their original pine host. However, because all receptor trees used in between-tree transfers occurred on a distant site from donor trees, the experimental design used to test for local adaptation was confounded with possible habitat effects (Kareiva 1982, Unruh and Luck 1987, Hanks and Denno 1993b).
We tested for local adaptation in the armored scale Pseudaulacaspis pentagona (Targioni-Tozzetti) by conducting within- and between-tree transfers of eggs and by measuring subsequent survivorship. In our design, however, all trees occurred within the same habitat (an urban landscape) and potential demic effects were not obscured by habitat differences. The influence of gene flow on local adaptation in P. pentagona was investigated by conducting intertree transfers (1) between neighboring trees (high gene-flow potential) and (2) between isolated trees (low gene flow). We hypothesized that local adaptation was more likely to occur on isolated than neighboring trees due to reduced gene flow and that transfer success would be higher on "near-tree" compared to "far-tree" transfers. To document that potential differences in P. pentagona survival between inter-tree transfers resulted from differences in tree characteristics rather than environment alone, transfer trees were cloned, grown in a common garden, and the transfers repeated on the clones.
NATURAL HISTORY OF PSEUDAULACASPIS PENTAGONA AND ITS HOST PLANT MORUS ALBA
Pseudaulacaspis pentagona is among the most damaging armored scale pests of ornamental and fruit trees throughout its nearly cosmopolitan distribution (North and South America, Europe, Africa, Asia, and Australia) (Gossard 1902, Howard 1912, Simmonds 1958, Bennett and Hughes 1959, Van Duyn 1967, Beardsley and Gonzalez 1975, DeBach and Rosen 1976, Johnson and Lyon 1988, Miller and Davidson 1990). P. pentagona, a native of China, was first recorded in the United States in Florida in the early 1900s (Gossard 1902) and is currently distributed from Florida west to Texas and north to Maryland and Tennessee (Davidson et al. 1983).
P. pentagona has been recorded feeding on 98 genera of host plants distributed among 55 plant families, but in Maryland, it is found primarily on the introduced white mulberry, Morus alba L., its native host in China (Murikami 1970, Hanks and Denno 1993a). White mulberries occur abundantly throughout the urban landscape of Maryland (Hanks and Denno 1993a). White mulberries reproduce sexually, are wind pollinated, and in the eastern United States are the product of interbreeding among a large variety of introduced cultivars (Williams 1982, Ottman 1987). Variability in fruit color and leaf form is extreme among individual mulberry trees growing in the field (Gleason and Cronquist 1963).
P. pentagona is restricted to the bark of its hosts, but can infest twigs and branches of all sizes including the trunk (Hanks and Denno 1993a). Mulberry trees in woodlots and forest habitats remain scale free due to the activities of generalist predators, and P. pentagona is relegated to trees in urban landscapes where populations are contagiously distributed and often reach extremely high densities (Hanks and Denno 1993a, c). In the urban landscape it is not uncommon to find trees with high densities near trees that are free of the scale. Furthermore, the performance (survivorship) of P. pentagona varies tremendously among mulberry trees in urban habitats when natural enemies are excluded (Hanks and Denno 1993c).
In Maryland, P. pentagona is trivoltine with peaks of adult abundance in June, August, and October (Hanks and Denno 1993a). Males die in the fall, and only fertilized adult females overwinter (Davidson et al. 1983). Spring oviposition occurs in late April. The average fecundity is [approximately equal to] 80 eggs per female and the primary sex ratio is 1:1 (Hanks and Denno 1993a). P. pentagona eggs are unique among insects in being color dimorphic; female eggs are coral in color while male eggs are white. This color difference persists into the first-instar crawler stage.
P. pentagona crawlers are active up to 24 h and disperse primarily within plants rather than by aerial movement among plants (Hanks and Denno 1993a). Although aerial dispersal does occur and is important in colonization of new hosts, dispersal between distant hosts is minimal (Hanks and Denno 1993b). Crawlers settle in cracks and other irregularities in the bark and insert their mouthparts. Feeding is restricted to woody tissues (Davidson et al. 1983), and both adults and nymphs feed on tissues in and surrounding the cambium (Hanks and Denno 1993a).
Settled female P. pentagona crawlers molt into sessile second instars, which subsequently molt into immobile adults. Adult females of P. pentagona are concealed by disc-shaped waxy covers that are appressed to the bark of their host trees. Male crawlers pass through four sessile instars and form an elongate cover, which hangs free of the bark before the insects molt into winged adults (Stoetzel 1976). Adult male scales are very weak fliers and are typically limited to passive downwind dispersal (Rice and Moreno 1970). Males of P. pentagona live for a maximum of 24 h (Bennett and Brown 1958) and locate the sessile females by pheromonal attraction (Heath et al. 1979). Males commonly mate immediately after emergence with nearby females (Hanks and Denno 1993a), and both sexes mate several times with different individuals (Van Duyn and Murphey 1971, Hanks and Denno 1993a). P. pentagona, like all armored scale insects, is haplodiploid due to the elimination of the paternal chromosome set during development of the male eggs; males are haploid (N = 8) while females are diploid (N = 16) (Bennett and Brown 1958).
STUDY SITE AND METHODS
All field experiments were performed on Pseudaulacaspis pentagona-infested mulberry trees growing in the urban landscape of College Park, Maryland, USA. Mulberry trees primarily colonize disturbed sites (roadsides, parking lots, highway medians, and hedgerows). Trees are found most often as isolated individuals, but stands composed of as many as 10 trees also occur.
Intra- and intertree transfers and the survival of P. pentagona
We examined local adaptation in P. pentagona by using a series of egg transfers between pairs of scale-infested mulberry trees. Following transfer, the survival of crawlers and adults was determined. Each tree in the pair served as both a "donor" (a source of eggs) and a "receptor" (a recipient of eggs). For each tree in the pair, we performed intra- and intertree transfers in such a way that each tree received eggs from its own population of scales as well as from the scale population on the other tree of the pair. Intertree transfers of eggs were conducted: (1) between neighboring pairs of trees ("near-trees" separated by [less than]5 m) and (2) between isolated pairs of trees ("far-trees" separated from the nearest mulberry tree by [greater than or equal to]300 m). We used five pairs of trees for each of the near-tree and far-tree transfer experiments. The 20 mulberry trees used in the transfer experiments ranged from 10 to 20 yr in age, averaging 61 [+ or -] 3.5 cm in basal circumference. Trees in the near-tree and far-tree experiments did not differ significantly in size ([F.sub.1,18] = 1.05, P [is greater than] 0.05), or in the density of their scale populations (means [+ or -] 1 SE, 0.97 [+ or -] 0.15 and 1.01 [+ or -] 0.15 scales/[cm.sup.2] for "near-tree" and "far-tree" study trees, respectively; means not significantly different, [F.sub.1,18] = 0.07, P [is greater than] 0.05).
For each tree of a pair we transferred 30 scale eggs (15 males and 15 females) into each of eight cages (see Cage construction, below, for design) that were arranged 1 cm apart in a continuous series along a branch. Four cages contained eggs originating from that same natal tree (intratree transfers), and the remaining four cages contained eggs originating from the other, novel tree of the pair (intertree transfers). We alternated the intra- and intertree transfer cages along one branch. The transfer series of 8 cages/branch was replicated on 6-9 different branches for each tree of the pair. We collected eggs used in transfers between pairs of trees from a minimum of five infested cuttings arbitrarily sampled from each tree of the pair. All transfers were performed during July and September 1987.
Ten days after egg transfer we removed cages, sexed the settled crawlers, and determined their survival through settling (crawler survivorship). The survival of the settled crawlers through adulthood (postcrawler survivorship) was determined by recaging each cohort and assessing their numbers at the end of the generation (after 30 d). Total survivorship (egg to adult) was also calculated.
The proportional survival (means of 4 cages/branch) was arcsine-transformed prior to analysis of variance (Sokal and Rohlf 1981, SAS Institute 1988). For both the near- and far-tree transfer experiments, at least 12 branches (6-9 from each tree of a pair) were used as replicates (random effect). Egg source (the Egg source term) was considered a fixed effect with two levels (intratree and intertree transfers). Five pairs of trees were used and data were analyzed as though each Tree pair was an independent experiment. The Source (treatment) effect was tested using the Branch (Tree pair) x Egg source effect as the error term. The Tree pair effect was tested with the Branch (Tree pair) effect [i.e., the effect of Branch within Tree pair] as the error term. Evidence for local adaptation would be provided by a significant Egg source term arising from higher scale survival in the intratree than the intertree transfer treatment. A significant Tree pair or Branch term would indicate that survival varied between pairs of trees or among branches within trees. Differences between tree pairs in the relative magnitudes of survivorship in intra- and intertree transfers would result in a significant Tree pair x Egg source interaction term. Data for males and female scale insects were analyzed separately.
Adaptation of P. pentagona to tree genotype
To test for the effects of host genotype on survival of P. pentagona transferred between trees, while controlling for environment, we cloned transfer trees and grew the clones in a common garden and repeated the scale transfers on the clones. However, because at least 2 yr are required to grow clones, we could only use clones of two study trees that had been established previously for other purposes. Because of limited sample size, the results of this study should be interpreted with caution. Cuttings (four per tree) were taken from both natal trees of one of the "far-tree" transfer pairs and used to establish eight clones in the greenhouse. Cuttings (50 cm in length x 1.5 cm in diameter) were rooted in pots containing a 1:1 mixture of peat moss and Perlite. In the greenhouse the clones were exposed to natural light, were watered daily to saturation, and were fertilized with Osmocote (14-14-14 NPK fertilizer, Sierra Chemical, Milpitas, California, USA). Clones were grown in the greenhouse for 2 yr. We collected eggs from each parent tree in the field and transferred eggs to its four clones (intratree-genotype transfer) and to the four clones of the other parent tree (intertree-genotype transfer). For each clone, three cages containing eggs (15 males and 15 females/cage) from the parent tree were alternated with three cages containing eggs from the non-parent tree. Cages were arranged 1 cm apart in a series along the trunk of the clone. We assessed crawler and postcrawler survival, 10 and 40 d respectively after the initiation of the experiment (14 August 1988), which allowed us to calculate total survival.
Mean survival values (three cages per clone) were arcsine-transformed prior to analysis of variance (Sokal and Rohlf 1981, SAS Institute 1988). Evidence for adaptation to host genotype would be provided by a significant Source effect arising from higher scale survival in the intratree-genotype than the intertree-genotype transfer treatment.
Transfer cages (2.5 [cm.sup.2]) were constructed from three squares of duct tape (Ace Hardware, Kensington, Illinois, USA) layered one on top of the other, adhesive side up. The bottom square was perforated with pin holes prior to assembly. Holes 1 cm in diameter were precut into the center of the two top squares of tape, creating a shallow depression into which a 1.5-cm-diameter disk of paper toweling was pressed. P. pentagona eggs were placed in this paper-lined well and were covered with a 1.5-cm-diameter disk of nylon organdy. A perimeter of exposed adhesive remained around the well, and the cage was inverted and pressed onto the bark of the branch. Upon hatching, crawlers passed through the organdy mesh and settled on the bark. Each series of eight cages used in the transfer experiments was covered with a tent of Parafilm to protect it from rain. Because cages effectively excluded predators and parasites, differences in mortality among treatments were host-plant related.
Intra- and intertree transfers and the survivorship of P. pentagona
Pseudaulacaspis pentagona (either sex) did not appear to be adapted to neighboring mulberry trees. Crawler, postcrawler, and total survival did not differ between scales raised on their natal tree and those transferred to and raised on a neighboring tree (nonsignificant Egg source term, Table 1). Total female survivorship and male survival (crawler, postcrawler, and total) were affected by branch. The crawler and postcrawler survival rate ranged from 0.16 to 0.53 for females and 0.25 to 0.72 for males, respectively, while total survival averaged 0.1 for females and 0.19 for males. Crawler and total survival (both sexes) and postcrawler (only males) survival differed significantly among pairs of trees used in the "near tree" transfer experiment (significant Tree pair term in Table 1). Cages on some branches were lost due to branches rubbing together, or crawlers failed to settle on some branches; thus, degrees of freedom are lower than in the original design.
In contrast, P. pentagona (both sexes) appeared to be adapted to individual isolated mulberry trees. Crawler and total survival (males and females) and postcrawler survival (males only) were higher for scales raised on their natal tree than for those scales transferred to and raised on a distant tree (significant Egg source term, Table 2). The postcrawler survival rate of females was higher on natal trees (0.61) than on distant trees (0.49), but these means were not significantly different. Crawler survival (both sexes) and male total survival was affected by both the tree pairs they were transferred to, branch effects, and the Tree pair x Egg source interaction. Female total survival was affected by the Egg source and Tree pair terms. Female postcrawler survival was affected only by the tree pair on which the scales were raised, while male postcrawler survival was TABULAR DATA OMITTED TABULAR DATA OMITTED affected by Branch effects and the Tree pair x Egg source interaction. The significant Tree pair x Egg source interaction term suggests that there was some variability in Egg source means across tree pairs.
TABLE 3. Crawler, postcrawler, and total survivorship of Pseudaulacaspis pentagona (mean proportion [+ or -] 1 SE for both sexes) raised on clones of a pair of mulberry trees in College Park, Maryland. Scale Tree genotype transfer Scale stage sex Intraclone Interclone Survivorship F 0.25 [+ or -] 0.06 0.27 [+ or -] 0.1 Crawler M 0.41 [+ or -] 0.07 0.41 [+ or -] 0.08 Postcrawler F 0.71 [+ or -] 0.09 0.75 [+ or -] 0.09 M 0.73 [+ or -] 0.07 0.65 [+ or -] 0.1 Total F 0.21 [+ or -] 0.06 0.22 [+ or -] 0.08 M 0.29 [+ or -] 0.06 0.27 [+ or -] 0.08
Adaptation of P. pentagona to tree genotype
Pseudaulacaspis pentagona were not adapted to host genotype alone when transfers were made between clones of two field trees from the "far-tree" experiment. Crawler, postcrawler, and total survivorship (both sexes) were not significantly different for scales raised on clones taken from their natal tree (intratree-genotype transfer) and clones taken from a distant tree (intertree-genotype transfer) (Table 3; nonsignificant Source term, Table 4). P. pentagona may not adapt to individual tree genotypes, but to tree phenotype.
TABLE 4. Analysis of variance results for crawler, postcrawler, and total survivorship (both sexes) of Pseudaulacaspis pentagona raised on clones taken from a pair of mulberry trees in College Park, Maryland. Each tree served as a "donor" (a source of eggs) and as a source of cloning stock. For clones from each tree in the pair, intratree- and intertree-genotype transfers were performed in such a way that each clone received eggs from its parent tree population of scales as well as from the scale population on the other tree of the pair. Survivorship Females Males Source ss df F P ss df F P Crawler Tree clone 376 1 1.34 NS(*) 355 1 2.38 NS Egg source 2.66 1 0.01 NS 0.41 1 0.001 NS Error 3088 11 1643 11 Postcrawler Tree clone 45 1 0.11 NS 664 1 3.24 NS Egg source 60.8 1 0.15 NS 129 1 0.63 NS Error 1283 6 2256 11 Total Tree clone 82 1 0.02 NS 14.4 1 0.10 NS Egg source 3.31 1 0.02 NS 15.6 1 0.10 NS Error 1465 9 1672 11 * NS = nonsignificant.
When host trees were well isolated from other host trees, survival of Pseudaulacaspis pentagona was significantly higher when raised on the natal host trees compared to rearings on novel trees. This finding is consistent with local adaptation of scale populations to individual host trees. That evidence for local adaptation was found for both sexes of P. pentagona argues against the hypothesis that ploidy differences between the sexes will render males poorer colonists of novel hosts (Alstad and Edmunds 1989). The clone experiment suggests that adaptation of P. pentagona to individual trees was not driven by tree genotype alone, but rather by tree phenotype. For example, edaphic effects on host trees can strongly affect the fitness of scale insects (e.g., Flanders 1970, McClure 1977a, Sheffer and Williams 1987) and might result in genetic differences between scale populations.
Local adaptation in populations of phytophagous insects on individual host plants has been examined using intra- and reciprocal interplant transfers in five other independent studies on relatively sedentary insects including the armored scale insect Nuculaspis californica Coleman (Rice 1983), the cryptococcid scale Cryptococcus fagisuga Lindinger (Wainhouse and Howell 1983), the margarotid scale Matsucoccus acalyptus Herbert (Unruh and Luck 1987, Cobb and Whitham 1993), and the thrips Apterothrips secticornis Trybom (Karban 1989). Evidence for local adaptation to host plants was found only for C. fagisuga and A. secticornis.
Our study of P. pentagona and that of C. fagisuga by Wainhouse and Howell (1983) provide evidence for the importance of host plant isolation in local adaptation. In both studies the experimental plants occurred in both adjacent and more isolated plantings (D. Wainhouse, personal communication). Evidence of deme formation in P. pentagona was detected only where hosts were isolated from other infested hosts. Similarly, evidence for local adaptation was found in beech scale when host trees were relatively isolated from other heavily infested trees, but was not in evidence when study trees stood adjacent to other infested trees in an orchard setting--providing some circumstantial evidence for the importance of isolation in deme formation (D. Wainhouse, personal communication).
Low herbivore mobility combined with host plant isolation could foster genetic differentiation of populations by reducing gene flow (Futuyma and Peterson 1985, Sturgeon and Mitton 1986, Smith 1988, Karban 1989, Alstad and Corbin 1990). Crawlers of both P. pentagona and C. fagisuga and adult males of P. pentagona have limited dispersal abilities (Wainhouse 1980, Hanks and Denno 1993a). C. fagisuga only occurs as parthenogenetic females (Wainhouse 1980), eliminating gene flow through male dispersal. The absence of local adaptation in other scale insects (N. californica and M. acalyptus) feeding on individual conifers (Rice 1983, Unruh and Luck 1987, Cobb and Whitham 1993) may be attributable to the occurrence of infested trees in proximity to the experimental trees. Even limited gene flow between herbivore populations on trees in contiguous stands could be sufficient to counter selection imposed by the host plant, especially if selection is weak (see Maynard Smith 1970, Felsenstein 1981).
Local adaptation may be encouraged by low density conditions characterized by increased inbreeding and restricted gene flow (Templeton 1980). Species experiencing violent population fluctuations and outbreaks, such as the scale species we discuss (Rice 1983, Wainhouse and Howell 1983, Unruh and Luck 1987, Hanks and Denno 1993a), may be subject to density-dependent dispersal, increased gene flow, and the swamping of genes directing local adaptation. For this reason, local adaptation of P. pentagona may be less pronounced on trees in urban settings than on trees in more natural habitats where natural enemies maintain scale densities at consistently low levels (Hanks and Denno 1993c).
A number of other genetic factors may limit the degree to which herbivores adapt to individual host plants. Restriction of gene flow among insect populations may also inhibit adaptation to host plants by limiting genetic variation upon which selection can act (Slatkin 1987). Variability in resistance properties within an individual host plant may select for a more general herbivore genotype and preclude the selection of a single genotype (Writham 1983). In addition, interplant variation may be too low to impose diversifying selection on herbivore populations (Futuyma and Peterson 1985). Our understanding of the influence of host plant genetics on the performance of P. pentagona is limited by the lack of information on the genetic relatedness of mulberry tree hosts. In our experiments the possibility remains that survival of scales was similar on novel and natal trees in the "near-tree" transfers because the neighboring trees were closely related to one another compared to the isolated trees of the "far-tree" transfers.
By adapting to individual plants, few populations of herbivores appear to sacrifice their ability to colonize new conspecific hosts. Local adaptation of herbivorous insects on individual hosts may be rare and seems more likely to occur in isolated populations of herbivores with poor dispersal ability. It is worth noting that all the herbivore species used to test the local adaptation hypothesis exhibit relatively low mobility (scale insects and apterous thrips). Despite this bias, evidence for local adaptation was found for only half of these cases. However, Mopper et al. (1995) have recently found evidence of local adaptation to host plant individuals in the leafmining moth Stilbosis quadricustatella, suggesting that fine-scale genetic differentiation is possible despite high potential gene flow resulting from movements of the more vagile adults.
While local adaptation appears to be a viable hypothesis for explaining patchy distributions of phytophagous insects on their host, other factors may play a greater role for most species of herbivores. Genetic variation in resistance traits among hosts may dictate a contagious herbivore distribution in the absence of local adaptation (Flanders 1970). For example, resistance properties of one clone line explained much of the patchy distribution of C. fagisuga in an orchard setting (Wainhouse and Deeble 1980, Wainhouse et al. 1988).
Environmental variation in host plant phenotype can also strongly affect the distribution of herbivores (Flanders 1970, McClure 1977b, 1986). Herbivores that are more intimately associated with their hosts (e.g., scale insects, borers, gall formers, leafminers) often show greater tree-to-tree differences in density than do foliage feeders due to environment-related variation in nutrients and defensive compounds (Mattson et al. 1988). For P. pentagona, water deficit greatly affects the distribution in urban habitats (Hanks and Denno 1993c). Lastly, mortality due to natural enemies may also affect the spatial distributions of scale insects. Specifically, mortality inflicted by generalist predators in forest habitats effectively restricts the distribution of P. pentagona to trees in urban landscapes (Hanks and Denno 1993c).
Local adaptation may serve to fine tune herbivore populations to individual host phenotypes, but may be unlikely to play a general role in explaining the patchy distribution of herbivorous insects on their host plants. While we have found evidence for local adaptation, this hypothesis cannot be used to explain the drastic differences in scale populations on neighboring trees. However, the combined influences of plant water relations and natural enemies confine populations of P. pentagona to a small subset of mulberry trees in the urban landscape and may better explain patchy scale distributions within stands of host trees (Hanks and Denno 1993c).
We appreciate the constructive comments of Donald Alstad, Neil Cobb, John Davidson, Irwin Forseth, Rick Karban, James Ott, Michael Raupp, and Rick Redak. Stanley Faeth, Susan Mopper, and an anonymous reviewer improved the clarity of the final draft. Partial support for this research was provided by the Gahan Regents Fellowship to L. M. Hanks. This is Scientific Article Number A6402, Contribution Number 8592 of the Maryland Agricultural Experiment Station, Department of Entomology.
Alstad, D. N., and K. W. Corbin. 1990. Scale insect allozyme differentiation within and between host trees. Evolutionary Ecology 4:43-56.
Alstad, D. N., and G. F. Edmunds, Jr. 1983. Adaptation, host specificity and gene flow in the black pineleaf scale. Pages 413-426 in R. F. Denno and M. S. McClure, editors. Variable plants and herbivores in natural and managed systems. Academic Press, New York, New York, USA.
Alstad, D. N., and G. F. Edmunds, Jr. 1989. Haploid and diploid survival differences demonstrate selection in scale insect demes. Evolutionary Ecology 3:253-263.
Alstad, D. N., G. F. Edmunds, Jr., and S. C. Johnson. 1980. Host adaptation, sex ratio, and flight activity in male black pineleaf scale. Annals of the Entomological Society of America 73:665-667.
Beardsley, J. W., Jr., and R. H. Gonzalez. 1975. The biology and ecology of armored scales. Annual Review of Entomology 20:47-73.
Bennett, F. D., and S. W. Brown. 1958. Life history and sex determination in the diaspine scale, Pseudaulacaspis pentagona Targ. (Coccoidea). Canadian Entomologist 90:317-324.
Bennett, F. D., and I. W. Hughes. 1959. Biological control of insect pests in Bermuda. Bulletin of Entomological Research 50:423-436.
Berenbaum, M. R., A. R. Zangerl, and J. K. Nitao. 1986. Constraints on chemical coevolution: wild parsnips and the parsnip webworm. Evolution 40:1215-1228.
Bush, G. L., and S. R. Diehl. 1982. Host shifts, genetic models of sympatric speciation and the origin of parasitic insect species. Pages 297-306 in Proceedings of the 5th International Symposium on Insect-Plant Relationships. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands.
Cobb, N., and T. Whitham. 1993. Herbivore deme formation on individual trees: a test case. Oecologia 94:496-502.
Davidson, J. A., D. R. Miller, and S. Nakahara. 1983. The white peach scale, Pseudaulacaspis pentagona (Targioni-Tozzetti) (Homoptera: Diaspididae): evidence that current concepts include two species. Proceedings of the Entomological Society of Washington 85:753-761.
DeBach, P., and D. Rosen. 1976. Armoured scale insects. Pages 139-178 in V. L. Delucchi, editor. Studies in biological control. International Biological Programme No. 9. Cambridge University Press, Cambridge, England.
Dickinson, H., and J. Antonovics. 1973. Theoretical considerations of sympatric divergence. American Naturalist 107:256-274.
Edmunds, G. F., and D. N. Alstad. 1978. Coevolution in insect herbivores and conifers. Science 199:941-945.
Felsenstein, J. 1981. Skepticism towards Santa Rosalia, or why are there so few kinds of animals? Evolution 35:124-138.
Flanders, S. E. 1970. Observations on host plant induced behavior of scale insects and their endoparasites. Canadian Entomologist 102:913-926.
Fritz, R. S. 1990. Effects of genetic and environmental variation on resistance of willow to sawflies. Oecologia 82:325-332.
Futuyma, D. J., and S. C. Peterson. 1985. Genetic variation in the use of resources by insects. Annual Review of Entomology 30:217-238.
Gleason, H. A., and A. Cronquist. 1963. Manual of vascular plants of the northeastern United States and adjacent Canada. Prindle, Weber & Schmidt, Boston, Massachusetts, USA.
Gossard, H. A. 1902. Two peach scales. Florida Agricultural Experimental Station Bulletin 61:492-498.
Hanks, L. M., and R. F. Denno. 1993a. The white peach scale, Pseudaulacaspis pentagona (Targioni-Tozzetti) (Homoptera: Diaspididae): life history in Maryland, host plants, and natural enemies. Proceedings of the Entomological Society of Washington 86:96-102.
Hanks, L, M., and R. F. Denno. 1993b. The importance of demic adaptation in colonization and spread of scale insect populations. Pages 393-411 in K. C. Kim, editor. Evolution of insect pests: patterns of variation. John Wiley & Sons, New York, New York, USA.
Hanks, L. M., and R. F. Denno. 1993c. Natural enemies and plant water relations influence the distribution of an armored scale insect. Ecology 74:1081-1091.
Hare, J. D. 1980. Variation in fruit size and susceptibility to seed predation among and within populations of the cocklebur, Xanthium strumarium L. Oecologia 46:217-222.
Hare, J. D., and D. J. Futuyma. 1978. Different effects of variation in Xanthium strumarium L. (Compositae) on two insect seed predators. Oecologia 37:109-112.
Heath, R. R., J. R. McLaughlin, J. H. Tumlinson, T. R. Ashley, and R. E. Doolittle. 1979. Identification of the white peach scale sex pheromone. Journal of Chemical Ecology 5:941-953.
Howard, L. O. 1912. The activity of Prospaltella berlesei Howard against Diaspis pentagona Targ. in Italy. Journal of Economic Entomology 5:325-328.
Johnson, W. T., and H. H. Lyon. 1988. Insects that feed on trees and shrubs. Cornell University Press, Ithaca, New York, USA.
Karban, R. 1987. Effects of clonal variation of the host plant, interspecific competition, and climate on the population size of a folivorous thrips. Oecologia 74:298-303.
-----. 1989. Fine-scale adaptation of herbivorous thrips to individual host plants. Nature 340:60-61.
Kareiva, P. 1982. Insects and adaptations. Book review. Science 215:658-659.
Levene, H. 1953. Genetic equilibrium when more than one ecological niche is available. American Naturalist 87:331-333.
Maddox, G. D., and R. B. Root. 1987. Resistance to 16 diverse species of herbivorous insects within a population of goldenrod, Solidago altissima: genetic variation and heritability. Oecologia 71:8-14.
Mattson, W. J., R. K. Lawrence, R. A. Haack, D. A. Herms, and P. Charles. 1988. Defensive strategies of woody plants against different insect-feeding guilds in relation to plant ecological strategies and intimacy of association with insects. Pages 3-38 in W. J. Mattson, J. Levieux, and C. Bernard-Dagan, editors. Mechanisms of woody plant defenses against insects: search for a pattern. Springer-Verlag, New York, New York, USA.
Maynard Smith, J. 1966. Sympatric speciation. American Naturalist 100:637-650.
-----. 1970. Genetic polymorphism in a varied environment. American Naturalist 104:487-490.
McClure, M. S. 1977a. Dispersal of the scale Fiorinia externa (Homoptera: Diaspididae) and effects of edaphic factors on its establishment on hemlock. Environmental Entomology 6:539-544.
-----. 1977b. Parasitism of the scale insects, Fiorinia externa (Homoptera: Diaspididae), by Aspidiotiphagus citrinus (Hymenoptera: Eulophidae) in a hemlock forest: density dependence. Environmental Entomology 6:551-555.
-----. 1986. Population dynamics of Japanese hemlock scales: a comparison of endemic and exotic communities. Ecology 67:1411-1421.
Miller, D. R., and J. A. Davidson. 1990. A list of the armored scale insect pests. Pages 299-306 in D. Rosen, editor. The armored scale insects--their biology, natural enemies and control. Volume B. Elsevier Science, Amsterdam, The Netherlands.
Miller, D. R., and M. Kosztarab. 1979. Recent advances in the study of scale insects. Annual Review of Entomology 24:1-27.
Mitter, C., and D. J. Futuyma. 1983. An evolutionary genetic view of host-plant utilization by insects. Pages 413-495 in R. F. Denno and M. S. McClure, editors. Variable plants and herbivores in natural and managed systems. Academic Press, New York, New York, USA.
Mopper, S., M. Beck, D. Simberloff, and P. Stiling. 1995. Local adaptation and agents of selection in a mobile insect. Evolution, in press.
Moran, N. 1981. Intraspecific variability in herbivore performance and host quality: a field study of Uroleucon caligatum (Homoptera: Aphididae) and its Solidago hosts (Asteraceae). Ecological Entomology 6:301-306.
Murikami, Y. 1970. A review of biology and ecology of diaspine scales in Japan (Homoptera, Coccoidea). Mushi 43:65-114.
Ottman, Y. 1987. Rediscovering the realm of fruiting mulberry varieties. Fruit Varieties Journal 41:4-7.
Rice, R. E., and D. S. Moreno. 1970. Flight of male California red scale. Annals of the Entomological Society of America 63:91-96.
Rice, W. R. 1983. Sexual reproduction: an adaptation reducing parent-offspring contagion. Evolution 37:1317-1320.
SAS Institute. 1988. SAS/STAT user's guide. Release 6.03 edition. SAS Institute, Cary, North Carolina, USA.
Service, P. M. 1984. Genotypic interactions in an aphid-host plant relationship: uroleucon rudbeckiae and Rudbeckia laciniata. Oecologia 61:271-276.
Sheffer, B. J., and M. L. Williams. 1987. Factors influencing scale insect populations in southern pine monocultures. Florida Entomologist 70:65-70.
Simmonds, F. J. 1958. The oleander scale, Pseudaulacaspis pentagona Targ. (Homoptera: Coccoidea) in Bermuda. Bermuda Department of Agriculture Bulletin 31.
Simms, E. L., and M. D. Rausher. 1987. Costs and benefits of plant defense to herbivory. American Naturalist 130: 570-581.
Slatkin, M. 1987. Gene flow and the geographic structure of natural populations. Science 236:787-792.
Smith, D. C. 1988. Heritable divergence of Rhagoletis pomonella host races by seasonal asynchrony. Nature 336:66-67.
Sokal, R. R., and F. J. Rohlf. 1981. Biometry. W. H. Freeman, New York, New York, USA.
Stephens, G. R., and D. A. Aylor. 1978. Aerial dispersal of red pine scale, Matsucoccus resinosae (Homoptera: Margarodidae). Environmental Entomology 7:556-563.
Stoetzel, M. B. 1976. Scale-cover formation in the Diaspididae (Homoptera: Coccoidea). Proceedings of the Entomological Society of Washington 78:323-331.
Strauss, S. Y. 1990. The role of plant genotype, environment and gender in resistance to a specialist chrysomelid herbivore. Oecologia 84:111-116.
Sturgeon, K. B., and J. B. Mitton. 1986. Allozyme and morphological differentiation of mountain pine beetles, Dendroctonus ponderosae Hopkins (Coleoptera: Scolytidae) associated with host tree. Evolution 40:290-302.
Tashiro, H., and C. Moffitt. 1968. Reproduction in the California red scale, Aonidiella aurantii. II. Mating behavior and post insemination female changes. Annals of the Entomological Society of America 61:1014-1020.
Templeton, A. R. 1980. Modes of speciation and inferences based on genetic distances. Evolution 34:719-729.
Unruh, T. R., and R. F. Luck. 1987. Deme formation in scale insects: a test with pinyon pine scale. Ecological Entomology 12:439-450.
Van Duyn, J. W. 1967. Observations on the life history and studies on control of white peach scale, Pseudaulacaspis pentagona (Targioni) (Homoptera, Coccoidea). Thesis. University of Florida, Gainesville, Florida, USA.
Van Duyn, J. W., and M. Murphey. 1971. Life history and control of white peach scale Pseudaulacaspis pentagona (Homoptera: Coccoidea). Florida Entomologist 54:91-95.
Wainhouse, D. 1980. Dispersal of first instar larvae of the felted beech scale, Cryptococcus fagisuga. Journal of Applied Ecology 17:523-532.
Wainhouse, D., and R. Deeble. 1980. Variation in susceptibility of beech (Fagus spp.) to beech scale (Cryptococcus fagisuga). Annales des Sciences Forestieres 37:279-289.
Wainhouse, D., I. M. Gate, and D. Lonsdale. 1988. Beech resistance to the beech scale: a variety of defenses. Pages 277-293 in W. J. Mattson, J. Levieux, and C. Bernard-Dagan, editors. Mechanisms of woody plant defenses against insects: search for a pattern. Springer-Verlag, New York, New York, USA.
Wainhouse, D., and R. S. Howell. 1983. Intraspecific variation in beech scale populations and in susceptibility of their host Fagus sylvatica. Ecological Entomology 8:351-359.
Whitham, T. G. 1983. Host manipulation of parasites: within-plant variation as a defense against rapidly evolving pests. Pages 15-41 in R. F. Denno and M. S. McClure, editors. Variable plants and herbivores in natural and managed systems. Academic Press, New York, New York, USA.
Williams, G. 1982. Mulberries. Pomona 15:140-146.
|Printer friendly Cite/link Email Feedback|
|Author:||Hanks, Lawrence M.; Denno, Robert F.|
|Date:||Dec 1, 1994|
|Previous Article:||Foraging theory, patch use, and the structure of a Negev Desert granivore community.|
|Next Article:||Plant production and soil microorganisms in late-successional ecosystems: a continental-scale study.|