Randall M. Cooper and Ronald D. Oetting University of Georgia College of Agriculture Experiment Station Georgia Station Experiment, GA 30212

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1 ADAPTATIONS OF SCALE INSECTS I TO HOST VARIABILITY' Randall M. Cooper and Ronald D. Oetting University of Georgia College of Agriculture Experiment Station Georgia Station Experiment, GA Abslract: Scale insects survive by adapting to the phenotypic characteristics of 8 single host plant upon which they spend their entire life cycle. Coccoids must overcome host phenoimmunity and genetic immunity_ Scales adapt to these defenses by being able to successfuuy reproduce in populations with low male frequencies and by fonning demes on individual hosts. Polyphagous coccoids show host preferences, and may exhibit morphological forms peculiar to each host species. Varied forms may also occur on different organs of 8 hosl Understanding interactions such as this between the Coccoidea. their hosts, and the environment, will racilitate our errorts to bring scale insects within the realm or integrated pest management. Key Words: Coccoidea, scale insects, plant-herbivore interaction!:!, pheno-immunity, genetic immunity, host rorms. J. Agric. Entomol. 3(2): (April 1986) Scale insects are noted for their extensive and sometimes bizarre adaptations to the plant parasitic regime. Their great variety of form, including sexual dimorphism, has enabled the Coccoidea to adapt to nearly all botanical habitats and feed on most plant organs. One of the most important trends in coccoid phylogenesis is the increasingly sessile nature of females in the more advanced families. The female body form conforming most thoroughly to a sedentary lifestyle is found in the largest family, the armored scales (Diaspididae). Although many coccoids move from one site to another at various times during their developmental cycles, armored scales are incapable of wandering once they settle and commence feeding. Thus, scale survival requires thorough adaptation to the phenotypic differences of each individual host. Some of these adaptations, including responses to host defenses, are the subject of this paper. Dispersal The means by which scale insects disperse detennines their probability of encountering potential hosts of different phenotypes or species. Because scales are notorious plant pests, many studies of scale dispersal have been conducted (McClure 1977a; Washburn and Washburn 1984; Moran et al. 1982). Scales spread principally by passive transport on infested plant material and as unsettled crawlers (first instars) (Beardsley and Gonzalez 1975). The wandering of crawlers generally serves to disperse young away [rom the mother onto new growth of the same host (Bennett and Brown 1958; Brown 1958) or between adjacent hosts if 1 HOMOPTERA: Coccoidea. 2 Presented in the Graduate Student Symposium "Insect Plant Interactions" at the Southeastern Branch Meeting or the Entomological Society or America, Greenville, SC, Accepted ror publication 31 January

164 J. Agric. Entomol. Vol 3. No.2 (1986) the plant crowns are in contact (Bodenheimer 1951). Wind, another important dispersal and mortality agent, permits short and/or long range transport.

2 164 J. Agric. Entomol. Vol 3. No.2 (1986) the plant crowns are in contact (Bodenheimer 1951). Wind, another important dispersal and mortality agent, permits short and/or long range transport. Crawlers of the ice plant scale, Pufuinariella mesembryanthemi (Vallot), exhibit active aerial dispersal behavior by standing on their hind legs and facing downwind until they are blown away (Washburn and Frankie 1981). Scale Adaptations to Pheno-immunity Even though scales can readily disperse to other hosts, many individuals remain on the same plant 8S their parents. An important factor in the success of the population when multiple generations occur on a plant is the continuing nutritional quality and vigor of the host. Scoles must be able to tolerate changes in the chemical and physical composition of the host's sap due to environmental influences, plant maturation and senescence. Environmental influences on host physiology can cause a phenomenon known as "pheno-immunity" (Thiem 1933), a "physiological resistance of a host plant to infestation by its indigenous coccid" (Flanders 1970). In some cases, this immunity is a permanent, local phenomenon, due to the host's physiological response to the prevailing climate (Compere 1935, 1940, 1961) and/or edaphic condit.ions (McClure 1977a). In other cases, the response is only temporary and induced by changing meteorological and edaphic conditions (Flanders 1970). Pheno-immunity affects scale reproduction, causing high mortality and a temporary inability to reproduce (Thiem 1938), or a change in the population sex ratio. For example, male production by the black scale, Saissetia oleae (Bernard). under field conditions is normally rare. However, in 1909 Quayle and Rust (1911) reported that males were especially abundant on some host species in several locations between San Diego and Santa Barbara, CA. It has been suggested that the weak diaspidid genetic sex detenninotion mechanism can be environmentally overriden (Hughes-Schraeder 1948; Beardsley and Gonzalez 1975). Scale Adaptations to Genetic Immunity Differential resistance to scale attack within a plant species may be genetic in origin. From observations over 5 yr of the reproductive success of black pineleaf scale, Nuculaspis californica (Coleman), on ponderosa pine, Pinus ponderosa (Laws), Edmunds and Alstad (1978) concluded that the trees sbow a complex intraspecific variation in their defensive phenotype. Resistance to coccoid attack was not environmentally induced because adjacent trees had great variation in scale population density. The immunity was also not pennanenl In severe outbreaks, scale-free trees eventually became infested. By transferring black pineleaf scales from infested to uninfested trees, Edmunds and AJstad (1978) showed that "selection over many generations results in scale insect populations which are increasingly adapted to the defensive character of their host tree." Edmunds and Alstad called these populations "demes." When black pinelenf scale demes were followed on several ponderosa pines, a relationship was found between sex ratio, male behavior, and the degree of adaptation to the host. Sex ratios were female-biased as predicted by theoretical models of the evolution of the sex ratio in deme-structured populations (Hamilton 1967). However, the data showed a female bias stronger than any model predictions (Alstad et al. 1980). Alstad et al. hypothesized that the female-biased ratios did not result from a variation between production of the sexes, but were caused by

COOPER: Adaptations of Scale Insects 165 survivorship differences. Nuculaspis californica females are diploid and thus heterozygous for some traits.

3 COOPER: Adaptations of Scale Insects 165 survivorship differences. Nuculaspis californica females are diploid and thus heterozygous for some traits. This may enable them to survive better than the haploid males during the early stages of population adaptation to a host. "As selection reduces genetic variance and the deme becomes better host fitted, male and female adaptations are more nearly equal." (Alstad et ai., 1980) Thus, male frequency should increase with time. This hypothesis was supported by data showing a higher percentage of males on trees with greater scale density, and presumably better insect adaptation (Spearman rank correlations, 1979: n = 11, P < 0.10; 1980: n ~ 18, P < 0.05). In addition, every tree sampled in both years showed a higher 1980 male frequency (sign test, n = 11, random probability < 0.01). Based on black pineleaf scale male capture data and other observations, Alstad et al. (1980) concluded that male mating behavior also was consistent with increasing adaptation to a host. Most scale mating was very localized, and thus reduced gene now between trees. This contributed to the differentiation of scale populations, Populations poorly fitted to their host had high male mortality which prompted more between-tree matings. This provided for new genetic combinations which might improve fitness. The tannin-like compounds of ponderosa pines (Edmunds and Alstad 1978), and the resinosis of red pine, Pinus resinosa Ait. (McClure 1977b) are examples of plant chemical defenses to which scales must adapt. Morphological features, such as epidennal characters, may also counter scale attack. Agarwal and Sharma (1961) studied the occurrence and abundance of sugarcane scale, Melanaspis glomerata (Green), on different varieties and ecotypes of sugar cane, Saccharum spontaneum L., and found a direct relationship between heavy attacks and a high stomatal density on the stem. Adaptations Related to Polyphagy Even greater host adaptability thon previously discussed is necessary when polyphagy is considered. Many coccoids are polyphagous and have adapted to interspecific phytochemical, morphological, and habitat differences. Preferences between host species occur, and may be evident in differences in fecundity (McClure 1983) or sex ratio (Voukassovitch 1933; Priesner 1938). An interspecific host preference is sometimes a local phenomenon mediated by climate. For example, black scale has a wide host range including citrus, but citrus is normally not a preferred host. However, in regions like parts of California, Chile, and Spain, black scale infestations of citrus can be severe. In these areas, Flanders (1970) believed citrus resistance to infestation was counteracted by especially favorable environmental factors. The climate was apparenuy unfavorable for citrus infestation in South Africa as Compere (1940) found citrus trees entirely free of black scale growing adjacent to oleanders (Nerium spp.) which were heavily infested. Smith and Compere (1928) reported that black scale on citrus seemed to be unusually responsive to slight weather variations. Different hosts can also cause life history variations for scales. Stoeuel and Davidson (1973) compared the life history of the obscure scale, Melanaspis obscura (Comstock), on white oak, Quercus alba L., and pin oak, Q. palustris Muenchhausen, and found an ca. 1 month lag in development of most stages on white oak as compared with development on pin oak. On white oak, settled crawlers were the overwintering stage, while on pin oak second instars overwinter. Stoetzel and Davidson concluded that the two populations were reproductively

166 J. Agric. EnLomol. Vol. 3, No.2 (1986) isolated. Although morphological differences between the populations could not be found, it appeared that two species were present) one of which was new.

4 166 J. Agric. EnLomol. Vol. 3, No.2 (1986) isolated. Although morphological differences between the populations could not be found, it appeared that two species were present) one of which was new. Many examples illustrating the alteration of coccoid morphology by host species are reported in the literature. Taxonomists confused by host forms have mistakenly named a new scale species or genus (Knipscher et al. 1976). Ebeling (1938) divided the effects of host species on coccoid phenotype into two categories: (1) physical. when a scale changes shape to correspond to certain structural pecularities of the host, and (2) physiological, when, consumed as food, the host affects certain physiological and morphological characteristics of the scale. He cited the conspicuous variety of forms of the European fruit lecanium scale, Lecanium corni Bouche, as a prime example of the latter category. Lecanium corni has a wide host range which includes Prunus spp. This scale, occurring on black locust, Robinia pseudoacacia L., was believed to be a different species, L. robiniarum Douglas. By transferring scales between host species, Marchal (1908) and Voukassovitch (1930) showed that L. robiniarum was rarely a host--induced fonn of L. comi. The very marked differences in external appearances of the scales (i.e. the gradation of convexity from a lateral view) on different hosts are shown in Fig. 1. The greatest similarity exists between individuals from hosts which are most closely related, such as the Prunus spp. (plum, apricot, and peach) of Fig. 1. Ebeling (1938) transferred L. comi from apricot, Prunus armeniaca L., to Chrishnasberry, Schinus terebinthl/olius Raddi, and from alder, Alnus spp., to apricot. He observed that these scales developed the host-form found on their new host rather than the form of their progenitors. ~ ~ ~ OI~ PLU~' ON APRICOT ON PEACH L::\ L:\ n ON QUINCE OI~ OAK ON t 1APLE /\ ~ H ON tladrone ON CIiRISTMASBERRY lmm Fig. 1. Cross sections of dried specimens of Lecanium comi Bouche showing differences in form on various host species. (With permission from Ebeling 1938).

5 COOPER: Adaptations of Scale Insects 167 The Influence of Feeding Location on Eurymerous Coccoids Many coccoids are eurymerous (i.e., they may feed successfully on more than one organ of their host) (Balachowsky 1932; Vayssiere 1926). In some eurymerous species. the location of the insect on the host plant may affect its morphological characteristics (Lupo 1943; Stafford and Barnes 1948; Takahashi 1953; Takagi and Kawai 1967; Tippins and Beshear 1970). Dimorphism is frequently the case, and also may be associated with the seasons. For example, females of Putnam's scale. Aspidiotus ancylus (Putnam), overwinter on twigs, and Bre distinctively different from the summer lear form (Fig. 2) (Stannard 1965). The factors affecting such changes have not been investigated, but the appearance of stem forms on senescing leaves and intermediate forms on petioles (Knipscher et al. 1976) suggests that the cause may be variations in the chemical nature of physiology of parts of the host plant (Miller and Kosztarab 1979). Danzig (1970) believed that nutritional differences in the sap of leaves and stems caused dimorphism. b Fig. 2. Aspidiatus ancylus (Putnam) showing pygidial lobes of (a) twig form and (b) leaf form; pygidial plates of (c) twig form and (d) leaf form. (With permission from Stannard 1965).

6 168 J. Agric. EntomoJ. Vol. 3, No.2 (1986) CONCLUSION The Coccoidea have developed an array of chromosome systems reflecting the diversity of their specializations and allowing fol' new host adaptations as required for survival (Brown 1977). Continued study of these adaptations and host defenses will assist plant breeders in developing scale-resistant varieties. Pheno-immunity, which sometimes may be as complete as genetic immunity (Thiem 1938), must also be considered in scale resistance. Environmental factors responsible for pheno-immunity and host quality might be manipulated to promote this resistance. For example, McClure (1980) demonstrated how nitrogen fertilization affected host suitability of Eastern hemlock, Tsuga canadensis Carriere, for elongate hemlock scale, Fiomia externa Ferris. Understanding interactions such as this between the Coccoidea, their hosts, and the environment, will facilitate our efforts to bring scale insects within the realm of integrated pest management. ACKNOWLEDGMENT I thank Drs. Ron Oetting, James O. Howell, and H. H. Tippins for their reviews and suggestions wit.h the preparation of this manuscript. REFERENCES CITED Agarwal, R. A, and D. P. Sharma Studies on some epidermal characters and hardness of sugarcane stem in relation to the incidence of scale insect: Mclanaspis glomerata (Green). Indian J. Entomol. 22: Alstad, D. N., G. F. Edmunds, Jr.. and S. C. Johnson Host adaptation, sex ratio, and flight activity in male black pincleaf scale. Ann. Entomol. Soc. Am. 73: Balachowsky, A Etude biologique des Coccides du bassin occidental de la Mediterranee. Encycl. Entomo!. Ser. A, Vol. 15. Beardsley, J. W., Jr., and R. H. Gonzalez The biology and ecology of armored scales. Annu. Rev. Entorno!. 20: Bennett, F. D., and S. W. Brown Life history and sex determination in the diaspine scale Pseudaulacaspis pentagona (Tar.). Can. Entomol. 90: Bodenheimer, F. S Citrus Entomology in the Middle East with Special References to Egypt, Iran, Irak, Palestine, Syria, Turkey. Junk, the Hague, 633 pp. Brown, C. E Dispersal of the pine needle scale, Phenacaspis pini{oliae (Fitch). Can. Entomol. 90: Brown, S. W Adaptive status and genetic regulation in major evolutionary changes of coccoid chromosome systems. Nucleus 20: Compere, H Exploratory search for natural enemies of red scale. Calif. Citrog. 20: Compere, H Parasiws of the black scale, Saissetia oleae, in Africa. Hilgardia 13: Compere, H The red scale and its natural enemies. Hilgardia 31: Danzig, E. M Synonymy of some polymorphous species of coccids. Zool. Zh. 49: Ebeling, W Host-detennined morphological variations in Lecanium corni. Hilgardia 11: l. Edmunds, G. F., Jr., and D. N. Alstad Coevolution in insect herbivores and conifers. Science 199: Flanders, S. E Observations on host plant induced behavior of scale insects and their endoparasites. Can. Entomol. 102: Hamilton, W. D Extraordinary sex ratios. Science 156:

COOPER: Adaptations of Scale I.nsecls 169 Hughes-Schmeder, S. 1948. Cytology of coccids. Advan. Genet. 2: 127-203. Knipscher. R. C., D. R. Miller, ond J. A. Davidson. 1976.

7 COOPER: Adaptations of Scale I.nsecls 169 Hughes-Schmeder, S Cytology of coccids. Advan. Genet. 2: Knipscher. R. C., D. R. Miller, ond J. A. Davidson Biosyslematics of Chiollospis nyssoe Comstock (Homoptera: Diaspididae). with evidence supporting leaf and bark dimorphism of the scale. Melanderia 25: I-3D. Lupo. V. 19;13. II Mytilococcus {icifuliae (Berlese) e una fanna esliva del M. coflchi{ormis (Gmelin). Boll. Lab Entomo!. Agrar. R. lnst. Superior Agric. Portici 5: Marchal, P Notes sur les cochenilles de J'Europe et du nord de l'afrique. Ann. Soc. Ent. Frnnce 77: l\ 1cClure, M. S. 1977a. Dispersal of lhe scale Piorinia exlerrra (Homoptera: Diaspididae) and effects of edaphic factors on its esw.blishment on hemlock. Environ. Entomol 6: McClure, M. S. 1977b. Population dynamics of the red pine scnle, Matsucoccus resiflosoe (Homoptera: Margarodidae): The innuence of resinosis. Environ. Entomol. 6: McClure, M. S Foliar nitrogen: A basis for hosl suitability for elongate hemlock scale, F'iorirlia exlerna (Hompotera: Dillspididae). Ecology 61: McClure, M. S Reproducl-iol1 lind adaptation of exotic hemlock scales (Homoptera: Diaspididac) on their new and native hosts. Environ. Entomol. 12: l\ tiller, D. R., and M. Kosztarab Recent advances in the study of scale insects. Annu. Rev. Entomol. 24: Moran, V. C., B. H. Gunn, and G. H. Walter Wind dispersal and settling of flrsl-inslar crawlers of the cochineal insect Dnctylopiu.'i austrinwi (Homoplera: Coccoidea: Dactylopiidae). Eca!. Entomol. 7: Priesner, H A brief nole of the relation between the physiological condition of plants and insect attack. Bull. Soc. Found ler Ent. 22: Quayle, H. J., and E. W. Rusl The black scale. Calif. Exp. Sm. (B) 223: Smith, H. S., and H. Compere A preliminary report on the insect parasites of the black scale. Saissetia oleae (Benmrd). Univ. Calif. Pubis. Eot. 4: Stafford, E. M., and D. F. Barnes Biology of the fig scale in California. Hilgardia 18: Stannard, L. J., Jr Polymorphism in the Putnam's scale, Aspidiotus OflCYc!US (Homoptera: Coccoidea). Ann. Enl.omol. Soc. Am. 58: Stoetzel, M. R, and J. A. Davidson Life history variations of the obscure scales (Homoptera: Diaspididae) on pin oak and white oak in Maryland. Ann. Entomol. Soc. Am. 66, Takahashi, R Dimorphism in some species of Chiono.5pis and Phenocaspis. Boll. Lab. Zoo!' Gen. Agr. Portici 33: Takagi, S., and S. Kawai The genera Chionaspis and Pseudaulacaspis with a criticism on Phe"ac(L'ipis. Insecta Matsumurana 30: Thiem, H Beitrag zur parthenogenese und Phonologie der Geschlechter von EulL'Conium comi Bouche (Coccidae). Z. Morph. OekoL Tiere 27: Thiem, H Ueber Bedingungen der Massenvennehrung von Inseklen. Arb. physio!. anzew Ent. Berl. 5: Tippins, H. H., and R. J. Beshear A new species of Chionaspis (Homoptera: Diaspididoc) from Betula nigra. Ann. Ent.omol. Soc. Am. 63: Vayssiere, P Contribution a I'elude biologique et systematique des coccidae. Ann. des Epil}hyties 12: Voukassovitch, P Sur la polyphugie de la cochenille Lecanium comi. Compl. Rend. Soc. BioI. Paris 104: Voukassovitch, P Sur une invasion de la cochenille, Lecanium corni, dans les pnmelaies Yougoslavcs. Congr. lnl. Ent. Paris (1932), v. 5, pp Washburn, J. 0., and G. W. Frankie Dispersal of A scale insect, Puluinariclla mesembry(lfithcmi (Homoptera: coccoidca), on iccplant in California. Environ. Entomo!. 10: Washburn, J. 0., and L. Washburn, Active aeriol dispersal of minute wingless arthropods: Exploitation of boundary-layer velocity gradient.s. Science 223:

Scale Insects. Hemiptera: Many families

Scale Insects. Hemiptera: Many families Scale Insects Hemiptera: Many families Soft Scales Armored Scales Some Important Armored (Hard) Scales in Colorado Oystershell scale Pine needle scale Scurfy scale Walnut scale San Jose scale Poplar scale