Part I. Infectious Diseases Diseases Caused by Fungi Fungi and oomycetes known to infect blueberry, cranberry, and lingonberry are also listed in the appendix. Readers will note that in both the appendix and the text, alternative names of fungi are identified exclusively as “synonyms,” rather than as specific life cycle stages (e.g., “anamorph,” “teleomorph”). This practice reflects the policy for naming fungi issued in 2011 by the International Botanical Congress: namely, that the use of multiple names for the same fungus be abandoned. (Readers interested in learning more about this policy are referred to the 2011 article by Hawksworth [see Selected Reference].) Going forward, accommodating this new policy may mean that
the most familiar names of some fungi will change. Changes to the names of fungi, as well as other updates to taxonomy and nomenclature, will be made in the Common Names of Diseases lists for blueberry, cranberry, and lingonberry, which are available on the website of The American Phytopathological Society. Selected Reference Hawksworth, D. L. 2011. A new dawn for the naming of fungi: Impacts of decisions made in Melbourne in July 2011 on the future publication and regulation of fungal names. IMA Fungus 2:155-162.
Blueberries (Highbush and Rabbiteye) Alternaria Leaf Spot and Fruit Rot A leaf spot disease of highbush blueberry caused by an Alternaria sp. was first observed in North Carolina in 1973. Alternaria spp. had been isolated from blueberry stems and leaves by several researchers, but they were considered secondary invaders. The fungus has since been widely recognized as a pathogen of blueberry, is worldwide in distribution, and is likely to be found wherever blueberries are grown. The disease was described on southern highbush blueberry in Argentina in 2004 and on highbush blueberry in China in 2006. The fungus also was identified as the principal cause of postharvest fruit decay of blueberries in North Carolina (United States) in 1971 and has been reported to cause a fruit rot in most blueberry- growing regions. The development of semiautomated sorting and packing equipment has increased the incidence of this and other postharvest rots because of increased handling and the contamination of surfaces with spores during the packing process.
this mycelium may completely engulf the berry by the time commercially packed fruit reach the consumer.
Causal Organism This leaf spot and fruit rot is caused by Alternaria tenu issima. Conidiophores (4–5 × 30–50 µm) are yellow-brown, simple, and smooth and have three to five septa, with slightly swollen tips. Conidia are dark, ovoid, obclavate, and pyriform and are muriformly divided with one to seven cross septa and one to three vertical septa; they are 7–15 × 15–55 µm (mean 10.8 × 35.8 µm). Beaks (spore tails) are cylindrical, 2–3 µm in diameter, and up to 15 µm long (Fig. 14). Colonies in culture are initially gray, becoming dark olive green with sporulation.
Symptoms Leaf lesions develop as circular to irregularly shaped, light brown to gray spots 1–5 mm in diameter surrounded by a brownish red border (Fig. 12). Lesions continue to enlarge when humidity is high but remain as small flecks when humidity is low. Flecking also occurs on stems. Symptoms of fruit infection develop when the fruit ripen. The calyx end of the berry is covered with closely appressed, greenish black fungal mycelium and spores (Fig. 13). After storage at room temperature for 10–20 h, fruit may become “leaky.” Postharvest infections appear as fluffy gray-green mycelium, often (but not exclusively) on the stem end of the berry. If berries are handled wet or are not kept cool after packing,
Fig. 12. Alternaria leaf spot, caused by Alternaria tenuissima, on blueberry leaves. (Courtesy R. D. Milholland; © APS)
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Disease Cycle and Epidemiology Alternaria leaf spot is a minor leaf disease that develops primarily during prolonged periods of cool, wet weather, when spores are produced in abundance. In most cases, only lower leaves are affected but, in rare cases, severe defoliation occurs. A. tenuissima overwinters in and on twigs and in debris on the ground. The fungus also readily colonizes freeze-and herbicide-injured shoots. The optimal temperature for growth and spore germination is 28°C; however, disease development is optimal at 20°C. In postharvest handling and packing facilities, spores from field-infected berries rapidly contaminate inspection belts and other handling surfaces. Healthy berries coming into contact with these surfaces pick up the spores, and even dry berries may become infected through wet stem scars.
Management Control of Alternaria leaf spot and preharvest fruit rot is essential to the delivery of high-quality blueberries to the market. Fungicides provide some control, but the primary means of controlling Alternaria fruit rot is through cultural practices, such as timely harvesting, dry handling, and rapid postharvest cooling. High levels of Alternaria fruit rot in the field are an indicator of berries that have been left on the bush too long. In North Carolina, highbush blueberries must be picked every 4–5 days and rabbiteye blueberries should be picked every 8–10
days. To avoid postharvest fruit rots, it is critical that berries are dry during harvesting and packaging. Because fungal spores need moisture to germinate and infect fruit, handling berries when they are wet with rain or dew greatly increases the chance of postharvest rots. Picking buckets, packing lines, and inspection belts should be cleaned frequently to reduce the chance of contamination by fungal spores and other microorganisms. Rapid forced-air cooling of fruit after harvest is necessary to dry the stem scars, retard fungal growth, and preserve the quality of harvested fruit. Cultivars that have a wet stem scar are more prone to postharvest infection and should be avoided. Selected References Cline, W. O. 1996. Postharvest infection of highbush blueberries following contact with infested surfaces. HortScience 31:981-983. Luan, Y. S., Feng, L., Xia, X. Y., and An, L. J. 2007. First report of Alternaria tenuissima causing disease on blueberry in China. Plant Dis. 91:464. Milholland, R. D. 1973. A leaf spot disease of highbush blueberry caused by Alternaria tenuissima. Phytopathology 63:1395-1397. Milholland, R. D., and Jones, R. K. 1972. Postharvest decay of highbush blueberry fruit in North Carolina. Plant Dis. Rep. 56:118-122. Wright, E. R., Rivera, M. C., Esperón, J., Cheheid, A., and Rodríguez Codazzi, A. 2004. Alternaria leaf spot, twig blight, and fruit rot of highbush blueberry in Argentina. Plant Dis. 88:1383.
(Prepared by R. D. Milholland; Revised by W. O. Cline)
Anthracnose Fruit Rot
Fig. 13. Alternaria fruit rot, caused by Alternaria tenuissima, on blueberry. (Courtesy W. O. Cline)
Blueberry anthracnose is one of the most economically important diseases of highbush, southern highbush, and rabbiteye blueberries. The disease is found in most growing areas of North America as well as several other continents. It has been reported most recently from Australia, Japan, New Zealand, Norway, Spain, and Switzerland. In addition, the primary causal organism, Colletotrichum acutatum, has been widely reported on other host species. While the disease can affect blossoms and shoots, its most destructive symptom is a rot of ripe fruit that may develop before or after harvest, from which its other common name, ripe rot, is derived. Anthracnose fruit rot is less common on lowbush blueberries. C. acutatum also causes a ripe rot of other fruit, nut, and vegetable crops, including almond, apple, avocado, citrus, cranberry, grape, mango, papaya, pecan, peppers, and strawberry. Although anthracnose fruit rot is widespread on commercial blueberries, losses vary greatly from region to region and from season to season. There is also significant variability in susceptibility among commercial cultivars. In Michigan (United States), for example, overall crop losses may range from 10 to 20%, depending on the season. The incidence of infection typically increases in successive pickings; in New Jersey (United States), losses exceeding 50% have been observed in the third picking. Ripe fruit may show symptoms of infection in the field, but most economic losses occur after harvest, when rot symptoms from latent infections develop on fruit in storage and spread to healthy fruit. Losses from postharvest rot may approach 100% under poor storage conditions.
Symptoms
Fig. 14. Conidia of Alternaria tenuissima, the causal organism of Alternaria leaf spot and fruit rot. (Courtesy W. O. Cline)
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Fruit rot is the most common and economically important stage of blueberry anthracnose. Fruit infections begin during bloom but infections remain latent and symptomless until the fruit ripen. The first symptom of infection may be shriveling of the berries on the bush. On overripe fruit, acervuli may form and exude sticky, salmon-colored conidial masses during warm, humid weather. Symptom development, however, may be delayed until fruit have been harvested and stored for a week
or more (Fig. 15). In storage, fruit rot typically begins at the blossom end of a berry, which softens and becomes sunken. Additional symptoms include blossom blight, but this symptom is rarely seen in the field except on susceptible cultivars under very humid conditions. Shoot tip blight (Fig. 16) and leaf spots may also develop during the growing season. Leaf lesions vary from small, brown, circular to irregularly shaped spots to large, black, poorly defined necrotic lesions. Shoot tip blight is common on succulent, rapidly growing shoots and may be more abundant on susceptible cultivars such as Coville and Bluecrop.
Causal Organisms Colletotrichum acutatum (syn. Glomerella acutata) is the species most often associated with anthracnose fruit rot on blue berries. It is a coelomycete fungus that produces fusiform, one- celled, hyaline conidia averaging about 3 × 14 µm. Conidia are produced on conidiophores in acervuli just below the epidermis of infected tissue and emerge as orange-to salmon-colored, sticky masses. On a berry, the acervuli sometimes grow in concentric rings, giving a lesion a bull’s-eye appearance. In culture, the fungus is often chromogenic when grown on standard growth media, such as potato dextrose agar. Blueberry isolates are typically deep red to light orange on the underside of the colony and white on top, although some include black or dark gray rays or sections.
C. gloeosporioides (syn. Glomerella cingulata) was considered the causal organism of anthracnose fruit rot in the original literature and is still found on rabbiteye and southern highbush blueberries in the southeastern United States but occurs less frequently than C. acutatum. C. gloeosporioides produces masses of sticky, salmon-colored conidia in acervuli formed on infected fruit and in culture. The conidia are hyaline, oblong- elliptical, and variable in size (average 4.7 × 10–28 µm) and shape but are usually rounded at the ends (Fig. 17). Some isolates of C. gloeosporioides from rotted fruit produce perithecia of G. cingulata. Perithecia are subspherical; asci (55 × 70 µm) are subclavate; ascospores are 3.5 × 12–22 µm. Fruit infected by C. gloeosporioides display symptoms similar to fruit infected by C. acutatum.
Disease Cycle and Epidemiology The fungus overwinters as mycelium in the bud scales surrounding floral and vegetative buds, blighted twigs, and fruit pedicels from the previous season. Conidia are dispersed from the overwintering sites to flower clusters and developing fruit (Fig. 18) either by splash dispersal or by epiphytic growth on the plant surface. Because fruit are susceptible to infection at all stages of development, the level of infection depends mainly on inoculum availability, cultivar susceptibility, and micro climate. Floral bud scales that persist on fruit clusters are believed to be an important source of initial inoculum because
Fig. 15. Symptoms of anthracnose fruit rot, caused by Colle totrichum acutatum, on harvested fruit. All blueberries were produced in commercial settings but with various levels of disease management. Note the pint on the right has nearly 100% anthracnose fruit rot. (Courtesy P. V. Oudemans; © APS)
Fig. 17. Conidia characteristic of Colletotrichum acutatum, the causal organism of blueberry anthracnose. (Courtesy P. V. Oudemans; © APS)
Fig. 16. Anthracnose shoot tip blight on blueberry, caused by Colletotrichum acutatum. (Cour tesy P. V. Oudemans; © APS)
Fig. 18. Blueberry fruit naturally infected with Colletotrichum acutatum, the causal organism of anthracnose fruit rot, with pedicels sporulating under laboratory conditions. (Courtesy P. V. Oudemans; © APS)
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of their proximity to developing fruit. The rate of bud scale dehiscence differs among cultivars and is related to field resistance; the faster these bud scales drop, the lower the incidence of fruit infection. Conidia germinate, produce germ tubes with melanized appressoria, and penetrate the cuticle through an infection peg. An infection hypha grows from the appressoria and ceases development until the fruit ripens. Infection requires a minimum of 8 h of continual leaf wetness at 25°C, with longer wetness durations needed at higher and lower temperatures. At 10°C, about 36 h of wetness are needed for infection. Sporulation on fruit is a major source of secondary inoculum. The optimal temperature for hyphal growth of the fungus is 26°C. Losses are most serious when there are prolonged periods of warm, wet weather during bloom and just before harvest.
Management The highbush cultivars Bluecrop, Bluetta, Cape Fear, and Coville are highly susceptible to the ripe rot fungus, whereas Elliott, Legacy, and Reveille exhibit resistance to infection. ‘Duke’ is considered only moderately resistant in controlled trials but exhibits significant field resistance under commercial growing conditions in New Jersey. Rabbiteye cultivars are generally far less susceptible, although differences among cultivars are evident. ‘Powderblue’, for instance, develops less ripe rot than ‘Premier’. Preharvest control of ripe rot on susceptible cultivars is best achieved with applications of an effective fungicide at 7-to 10- day intervals, beginning at full bloom. Postharvest disease development can be reduced by timely harvests, rapid postharvest cooling, and sanitation of sorting lines. Fungicide applications should be initiated during early bloom. Broad-spectrum fungicides (such as captan, fluazinam, and ziram) and more selective fungicides (such as the strobilurins) are very effective. Demethylation inhibitor (DMI) fungicides are variable in performance against these pathogens. Delayed dormant sprays with lime sulfur or captan reportedly help reduce overwintering inoculum. Selected References Daykin, M. E., and Milholland, R. D. 1984. Infection of blueberry fruit by Colletotrichum gloeosporioides. Plant Dis. 68:948-950. DeMarsay, A. 2005. Anthracnose fruit rot of highbush blueberry: Biology and epidemiology. Ph.D. dissertation. Rutgers University, New Brunswick, NJ. Hartung, J. S., Burton, C. L., and Ramsdell, D. C. 1981. Epidemiological studies of blueberry anthracnose disease caused by Colletotrichum gloeosporioides. Phytopathology 71:449-453. Polashock, J. J., Ehlenfeldt, M. K., Stretch, A. W., and Kramer, M. 2005. Anthracnose fruit rot resistance in blueberry cultivars. Plant Dis. 89:33-38. Smith, B. J., Magee, J. B., and Gupton, C. L. 1996. Susceptibility of rabbit eye blueberry cultivars to postharvest diseases. Plant Dis. 80:215-218. Verma, N., MacDonald, L., and Punja, Z. K. 2007. Environmental and host requirements for field infection of blueberry fruits by Colletotrichum acutatum in British Columbia. Plant Pathol. 56:107-113. Wharton, P. S., and Schilder, A. C. 2008. Novel infection strategies of Colletotrichum acutatum on ripe blueberry fruit. Plant Pathol. 57:122-134. Yoshida, S., Tsukiboshi, T., Shinohara, H., Koitabashi, M., and Tsushima, S. 2007. Occurrence and development of Colletotrichum acutatum on symptomless blueberry bushes. Plant Pathol. 56:871-877.
can attack fruit trees, strawberry, raspberry, blackberry, and grape. To date, Armillaria spp. have been reported as pathogens of highbush blueberry only in the United States and Italy. Many observations of the disease have probably gone unreported, particularly because the symptoms are easily confused with other problems. Although the disease is uncommon, it can cause serious damage in fields where it is found, and it is very difficult to control. The pathogen is sometimes referred to as the honey fungus, oak root fungus, oak fungus, and shoestring fungus. The disease is most likely to be found on sites where an oak forest has been cleared for planting.
Symptoms Infected bushes may display a range of symptoms. Plants low in vigor may appear to be suffering from nutritional disorders or a pH imbalance and may slowly decline in vitality over several years. Infected plants have small, chlorotic leaves and may be more susceptible to drought stress and winter injury than healthy plants. Branches may wilt suddenly, and the entire plant may die within a short time period. Affected bushes may be distributed in patches around focal points of fungal inoculum. The disease may be confined to one area of a field (Fig. 19) or it may be interspersed throughout the field, depending on the distribution of the primary inoculum. The most reliable diagnostic procedure is to scrape away the outer bark of the trunk and larger roots at or slightly below the soil line to examine the base of the affected bush. The fungus produces white mycelial fans (Fig. 20) between the bark and the hardwood, and striations may be present. Plants killed several months before examination may also have the mycelium of secondary invading fungi. Rhizomorphs—black, rootlike structures that also resemble shoestrings (Fig. 21)—may be attached to the roots or trunk, or they may be found growing freely in the soil. The fungus may produce mushroom fruiting bodies (Fig. 22) at the base of affected plants during late summer to early autumn if temperature and moisture conditions are right. These mushrooms are typically yellowish brown (honey colored), with a conspicuous ring around the stem below the cap. Because the mushrooms are frequently not produced, the mycelial fans and rhizomorphs are more reliable diagnostic features of the disease.
Causal Organisms Very little is known about the identity of the Armillaria spp. that cause root rot in blueberry. The most important species is
(Prepared by R. D. Milholland; Revised by A. DeMarsay and P. V. Oudemans)
Armillaria Root Rot Armillaria root rot is an important disease worldwide; it affects more than 500 species of woody plants. The causal fungus 12
Fig. 19. Highbush blueberry bushes affected by Armillaria root rot, caused by an Armillaria sp., in the field. (Courtesy A. M. C. Schilder; © APS)
Fig. 21. Rhizomorphs of an Armillaria sp. attached to an Armillaria root rot-infected blueberry root. (Courtesy T. D. Miles; © APS) Fig. 20. Mycelial fan of an Armillaria sp. in an Armillaria root rot-infected highbush blueberry plant. (Courtesy A. M. C. Schilder; © APS)
probably A. mellea, although A. ostoyae and A. gallica also have been isolated from infected bushes. All belong to the order Agaricales in the phylum Basidiomycota. Mushroom caps are 2–25 cm in diameter; however, they are usually produced in a dense clump and tend to be on the smaller end of this scale. The fruiting bodies darken with age; fresh mushrooms are easier to identify. It is easier to culture the fungus from fresh hyphal fans than from wood. The fungus often produces light to dark brown rhizomorphs in culture. Polymerase chain reaction is necessary to confirm the species.
Disease Cycle and Epidemiology Armillaria root rot is most likely to occur in recently cleared fields that have sandy, well-drained soil. Armillaria spp. survive in the soil on the debris of susceptible host plant roots. Blueberry roots that come in contact with this colonized food base are colonized by direct mycelial contact or from rhizomorphs. The fungus spreads further by root-to-root contact between infected and healthy bushes. The fungus can also survive on wood chip mulches. Spores disseminated from the mushrooms (basidiospores) are probably not important in the spread of the pathogen within a field. If the fungus remains confined to the roots, plants die slowly over several years. If the fungus invades the trunk, the plants are girdled and killed in a short time period.
Management When a forested location is to be used for planting, particularly where oak is an important species, the soil should be thoroughly disked and as many root fragments as possible should be removed. The area should be left fallow for at least 3 years so that the amount of inoculum of Armillaria spp. is significantly reduced. Soil fumigants or sterilants such as carbon disulfide are effective; however, if they do not penetrate deeper than 50 cm, some inoculum may remain in the soil. Armillaria spp. may be significantly weakened by the treatments, however, and may be attacked by Trichoderma spp. and other antagonistic fungi in the soil, thus further reducing inoculum potential. If the area to be planted is large, a few bushes planted in various locations 1 or 2 years after clearing might serve as a test of the degree of soil inoculum. Infected bushes should be removed and burned. A bush from beyond the disease perimeter that appears healthy should also be examined and should be removed if rhizomorphs and
Fig. 22. Basidiocarps of an Armillaria sp. at the base of an Armillaria root rot-infected highbush blueberry plant. (Courtesy F. L. Caruso; © APS)
mycelial fans are present at the root collar. Soil fumigation of areas where infected bushes have been removed helps to prevent recurrence of the disease in replanted areas. Wood chip mulch should be removed from healthy bushes around the disease centers and should not be replaced as long as there are rhizomorphs growing in the chips or at the mulch–soil line. No information is available on cultivar susceptibility to Ar millaria root rot. Most cultivars are probably highly susceptible to the fungus. Selected References Eglitis, M., Gould, C. J., and Johnson, F. 1966. Fungi found on Ericaceae in the Pacific coastal area. Wash. State Agric. Exp. Stn. Bull. 675. Fulton, R. H. 1958. New or unusual small fruit diseases and disease- like occurrences in Michigan. Plant Dis. Rep. 42:71-73. Munnecke, D. E., Kolbezen, M. J., Wilbur, W. D., and Ohr, H. D. 1981. Interactions involved in controlling Armillaria mellea. Plant Dis. 65:384-389. Prodorutti, D., Palmieri, L., Gobbin, D., and Pertot, I. 2006. First report of Armillaria gallica on highbush blueberry (Vaccinium corymbosum) in Italy. Plant Pathol. 55:583. Shaw, C. G., III, and Kile, G. A. 1991. Armillaria root disease. U. S. Dep. Agric. For. Serv. Agric. Handb. 691.
(Prepared by F. L. Caruso) 13
Botryosphaeria Stem Blight Botryosphaeria stem blight, commonly referred to as dieback, is a destructive disease of highbush and rabbiteye blue berries, primarily in the southeastern United States extending north into New Jersey. Losses are most severe in young fields, where plants often become infected and die in the first 2 years. In older fields, stem blight is most commonly seen as a dieback on one or more canes in a bush. A dramatic increase in stem blight incidence over the past 50 years has been associated with an increase in mechanized harvesting and mechanized pruning and a shift to more susceptible cultivars. Stem blight is also a major disease of low-chill southern highbush cultivars grown in the Gulf south. Besides blueberry, the disease affects other fruit crops, including apple, blackberry, peach, and citrus, as well as many other woody plants in temperate and tropical zones around the world.
Symptoms and Host Susceptibility The point of initiation of most stem blight infections is a wound on stems or canes. During the early stages of infection, characteristic symptoms are yellowing and reddening or drying of the leaves on one or more branches. A rapid wilt of leaves on individual branches is often followed by death of the entire
Fig. 23. Botryosphaeria stem blight on blueberry, caused by Botryosphaeria dothidea. (Courtesy R. D. Milholland; © APS)
Fig. 24. Cross section of a blueberry stem infected with Botryosphaeria dothidea, the causal organism of Botryosphaeria stem blight, showing brown discoloration of the infected wood. (Cour tesy P. V. Oudemans; © APS)
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plant as the fungus spreads downward through vascular tissue to the base of the plant. The most conspicuous symptom, called flagging, is a dead branch with leaves still attached in close proximity to living branches (Fig. 23). A stem blight-infected stem has a uniform, light brown discoloration in the wood extending down the infected side of the stem from a few centimeters to the entire length (Fig. 24). Twig infections may be confused with winter injury or other twig diseases. The infection can also develop in wounds at the base (crown) of the bush in susceptible cultivars, resulting in rapid plant death without the typical flagging symptoms associated with infections on individual stems. Younger plants die rapidly within 1–2 years of planting, and the mortality rate is highest when infection develops at or near the crown (Fig. 25). Stem blight infections usually become evident soon after harvest, and new infections can be observed throughout the summer months. Infections are often associated with wounds caused by mechanical damage, contact herbicide injury, insect damage, or late-season cold injury on succulent shoots that happened during the previous growing season. Temperatures below –18°C (0°F) may cause cracking in the forks on blue berry stems, which has resulted in wound-related epidemics the following spring. The greatest incidence of stem blight in New Jersey was found in years following winter injury. Drought stress also predisposes plants to stem blight. Fields that are irrigated regularly during dry periods have a much lower incidence of death and stem blight symptoms on infected plants than do fields that do not have sufficient and consistent soil moisture. On rabbiteye cultivars, stem blight infection usually is limited to dieback of individual canes or twigs, with an occasional major cane dying back to the ground, and it does not typically cause plant death except in young, vigorous plants. However, many mature rabbiteye plants in south Mississippi (United States) died during the spring following extensive bush damage caused by hurricanes the previous summer. Rabbiteye cultivars also show an increase in disease severity following exposure to stresses such as heat, drought, or cold. Blueberry cultivars vary widely in their response to infection by Botryosphaeria dothidea, and isolates of the pathogen show a broad range of pathogenicity. Most highbush cultivars grown in the southern United States are susceptible to B. do thidea. Field observations in North Carolina (United States) indicate that the highbush cultivars Bluechip and Bounty are very susceptible to stem blight. ‘Croatan’, ‘Reveille’, ‘Harrison’, and ‘Bladen’ and the rabbiteye cultivars Premier and Powderblue are also susceptible; however, plant losses of these cultivars average less than 10–20%. The highbush cultivars Murphy, Cape Fear, and O’Neal have shown field resistance in North Carolina with few plant deaths, although occasionally they do become
Fig. 25. Young blueberry plants showing symptoms of Botryo sphaeria stem blight, caused by Botryosphaeria dothidea. (Cour tesy R. D. Milholland; © APS)