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Plant-Parasitic Algae (Chlorophyta: Trentepohliales) in American Samoa1

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Plant-Parasitic Algae (Chlorophyta: Trentepohliales) in American Samoa1 Plant-Parasitic Algae (Chlorophyta: Trentepohliales) in American Samoa1 Fnd E. Erooks 2 Abstract: A survey conducted betweenJune 2000 and May 2002 on the island of Tutuila, American Samoa, recorded filamentous green algae of the order Tren­ tepohliales (CWorophyta) and their plant hosts. Putative pathogenicity of the parasitic genus Cephaleuros and its lichenized state, Strig;ula, was also inves­ tigated. Three genera and nine species were identified: Cephaleuros (five spp.), Phycopeltis (two spp.), and Stomatochroon (two spp.). A widely distributed species of Trentepohlia was not classified. These algae occurred on 146 plant species and cultivars in 101 genera and 48 families; 90% of the hosts were dicotyledonous plants. Cephaleuros spp. have aroused worldwide curiosity, confusion, and con­ cern for over a century. Their hyphaelike filaments, sporangiophores, and as­ sociated plant damage have led unsuspecting plant pathologists to misidentify them as fungi, and some phycologists question their parasitic ability. Of the five species of Cephaleuros identified, C. virescens was the most prevalent, followed by C. parasiticus. Leaf tissue beneath thalli of Cephaleuros spp. on 124 different hosts was dissected with a scalpel and depth of necrosis evaluated using a four­ point scale. No injury was observed beneath thalli on 6% of the hosts, but full­ thickness necrosis occurred on leaves of 43% of hosts. Tissue damage beneath nonlichenized Cephaleuros thalli was equal to or greater than damage beneath lichenized thalli (Strig;ula elegans). In spite of moderate to severe leaf necrosis caused by Cephaleuros spp., damage was usually confined to older leaves near the base of plants. Unhealthy, crowded, poorly maintained plants tended to have the highest percentage of leaf surface area affected by TrentepoWiales. Parasitic algae currently are not a problem in American Samoa because few crops are affected and premature leaf abscission or stem dieback rarely occur. PREVIOUS REPORTS of plant-parasitic algae (Chlorophyta) that are aerial rather than in American Samoa were limited to an un­ aquatic, brightly colored by orange carot­ identified species of Cephaleuros Kunze in enoid pigments, and uncommon in appear­ Fries, 1827, on mango (Mangifera indica L.), ances and lifestyles. A study of this order was guava (Psidium g;uajava L.), and avocado (Per­ initiated in 2000 based on a grower's anxiety sea americana Mill.) (McKenzie 1996). Cepha­ over orange, downy growths covering mango leuros is a member of the Trentepohliales, and guava leaves. It was also a response to a unique order of filamentous green algae previous authors who hoped to stimulate continued work on these interesting organ­ I Funded by the U.S. Department of Agriculture, isms (Joubert and Rijkenberg 1971) and to Cooperative State Research, Education and Extension document existing species of Cephaleuros in Service (USDA CSREES, Project SAM-020). Manu­ the Tropics before their hosts and habitats script accepted 1 August 2003. 2 Plant Pathologist, American Samoa Community were destroyed by population growth (Chap­ College Land Grant Program, P.O. Box 5319, Pago man and Good 1983). The goal ofthis project Pago, American Samoa 96799 (phone: 684-699-1394; fax: was to increase our knowledge of algae in 684-699-5011; e-mail: [email protected]). the Trentepohliales still existing in American Samoa. Pacific Science (2004), vol. 58, no. 3:419-428 The Trentepohliales currently comprises © 2004 by University of Hawai'i Press six genera (Thompson and Wujek 1997). All rights reserved Cephaleuros grows beneath the host's cuticle 419 420 PACIFIC SCIENCE· July 2004 and is considered an obligate epiphyte and cies, including C. virescens, grow beneath the occasional parasite by some (Thompson and plant's cuticle but above the epidermis and Wujek 1997) and a plant pathogen by others may cause little or no damage to the host. (Cunningham 1879, Marlatt and Alfieri Stomatochroon can cause incidental water­ 1981, Holcomb 1986, Holcomb et al. 1998). soaking of tissues but is not usually consid­ Stomatochroon Palm, 1934, lives in the sub­ ered a plant parasite. stomatal chambers of its host and was de­ Cephaleuros virescens is the most frequently scribed as an "obligate endophyte (parasite)" reported algal pathogen of higher plants by Chapman and Good (1983) and a com­ worldwide and has the broadest host range mensal organism by Timpano and Pearlmut­ (Joubert and Rijkenberg 1971, Marlatt and ter (1983). Phycopeltis Millardet, 1870, and Alfieri 1981, Chapman and Good 1983, Hol­ Physolinum Printz, 1921, are supracuticular comb 1986, Thompson and Wujek 1997). It epiphytes but may be found on other sur­ usually occurs on the upper leaf surfaces of faces under very humid or moist conditions perennial dicotyledonous plants, but its thalli (Thompson and Wujek 1992, Davis and occasionally are found on lower leaf sur­ Rands 1993, Rindi and Guiry 2002). The faces and on monocots (Joubert and Rij­ free-living algae Trentepohlia Martius, 1817, kenberg 1971, Chapman and Good 1983). and Printzina Thompson & Wujek, 1992, The roughly circular thalli appear velvety due occur widely on living and nonliving sub­ to setae (sterile hairs) and sporangiophores strates (Chapman 1984, Rindi and Guiry erupting through the host cuticle. The 2002, Thompson and Wujek 1992). hematochrome pigments astaxanthin and {3­ Few plant pathologists have the opportu­ carotene (Thompson and Wujek 1997, nity to identify plant-pathogenic Trente­ Lopez-Bautista et al. 2002) color the Trente­ pohliales as causal agents of disease for several pohliales yellow green to dark reddish or­ reasons. First, these algae are found mainly ange, reportedly due to changes in light, in tropical and subtropical climates (Chap­ temperature, and available nutrients (Joubert man and Good 1983, Thompson and Wujek et al. 1975, Lorenz 1999). 1992). Second, though they have a broad The nonintercellular, subcuticular species host range, their damage is often minimal and of Cephaleuros may not induce an obvious the presence of a few small thalli on leaves response on some hosts (Chapman 1984, or stems may go unnoticed (Joubert and Thompson and Wujek 1997). On other hosts, Rijkenberg 1971, Holcomb 1986). Finally, however, cell death occurs beneath the algal algae in this order are sometimes mistaken thallus (Thomas 1913, Joubert and Rijken­ for fungi due to their filamentous nature and berg 1971, Chapman and Good 1983, Hol­ formation of setae, sporangiophores, and comb 1986). There may be tissue hyperplasia, zoospores (Cunningham 1879, Singh 1962, with or without the formation of suberin, Wellman 1965, Chapman 1984, Holcomb either below or at the margins of lesions and Henk 1984, Reynolds and Dunn 1984). (Joubert and Rijkenberg 1971, Thompson Misidentification is enhanced when fungi and Wujek 1997). Stem infections have been invade these algae, forming lichens such as implicated in twig death and branch dieback Strigula and Raciborskiella (Santesson 1952, (Ruehle 1936, Knoor 1964, Chapman and Joubert and Rijkenberg 1971, Chapman and Good 1983, Holcomb 1986, Holcomb et al. Good 1983, Thompson and Wujek 1997). 1998) and algal spots on guava, avocado, and Cephaleuros is the genus commonly linked citrus fruits may reduce their marketability to plant damage (Joubert and Rijkenberg (Winston 1938, Ruehle 1941, Joubert and 1971, Marlatt and Alfieri 1981). Four of Rijkenberg 1971, Chapman and Good 1983). the 13 most damaging species grow inter­ Reports have described Cephaleuros spp. as cellularly: C. biolophus Thompson & Wujek, causal agents of disease for over a century C. minimus Karsten, C. parasiticlts Karsten, (Cunningham 1879, Ruehle 1936, Winston and C. pilosa Thompson & Wujek (Thomp­ 1938, Crandall and Davis 1944). Steps to son and Wujek 1997). The other nine spe- confirm its role as a plant pathogen (Koch's Plant-Parasitic Algae in American Samoa . Brooks 421 postulates), however, have not been com­ Two methods were used to estimate dis­ pleted. This is probably due to the difficulty ease severity caused by Cephaleuros spp. First, in producing zoospores for reinoculation on the most seriously affected host leaves were artificial media (Chapman and Good 1983, assessed by estimating the percentage of their Holcomb et al. 1998). upper leaf surfaces covered with algae: light The objectives of this study were to iden­ «5%), moderate (6-25%), or heavy (>25%). tify existing species of Trentepohliales in Disease severity was also measured for mature American Samoa and record their host range. thalli from a nonrandom sample of hosts us­ The emphasis of this report, however, is ing a four-point necrosis index: (0) no necro­ on Cephaleuros spp. and their reputed role as sis; (1) superficial necrosis of the cell layer plant pathogens. beneath the algal thallus, with or without tis­ sue hyperplasia; (2) necrosis of > 1 cell layer but not full leaf thickness, with or without MATERIALS AND METHODS tissue hyperplasia, erosion, or suberin forma­ Specimens were collected between June 2000 tion; and (3) necrosis from upper to lower and May 2002 from a wide range of plant leaf surface, including "shot-hole" symptoms. species on Tutuila, main island of the U.S. Damage was assessed under a stereoscope by Territory of American Samoa. Tutuila is lo­ dissecting fresh and dried lesions with a scal­ cated at approximately 14° 18' S latitude and pel. 170° 41' W longitude, has a mean annual Lichens with mature fruiting bodies and temperature of 26.4°C, and annual rainfall a species of Cephaleuros as the algal partner from 2,500 mm at lower elevations to over were recorded and sent to a lichenologist (c. 6,000 mm on Matafao Peak (660 m). Genera Smith, University of Hawai'i) for identifica­ of the Trentepohliales sometimes can be tion. Tissue damage beneath lichen thalli was identified in the field with a hand lens, but assessed with the necrosis index and com­ all specimens were taken to the laboratory for pared with damage by nonlichenized thalli on species determination by stereo- and light the same host. microscopy. Several factors make species identification difficult.
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