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Home , Cephaleuros, Cephaleuros parasiticus, Cephaleuros virescens, Plant pathology, Trentepohliaceae, Trentepohliales

-Parasitic (: ) 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 of the order Tren­ tepohliales (CWorophyta) and their plant hosts. Putative pathogenicity of the parasitic and its lichenized state, Strig;ula, was also inves­ tigated. Three genera and nine species were identified: Cephaleuros (five spp.), (two spp.), and Stomatochroon (two spp.). A widely distributed species of was not classified. These algae occurred on 146 plant species and in 101 genera and 48 families; 90% of the hosts were dicotyledonous . 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. 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 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 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 carot­ identified species of Cephaleuros Kunze in enoid pigments, and uncommon in appear­ Fries, 1827, on (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 , 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 and Wujek 1997) and a plant 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 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 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 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 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, (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 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 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 . 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 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. The historical use of RESULTS different morphological characters to distin­ guish between species has led to incorrect Cephaleuros, Stomatochroon, Phycopeltis, and descriptions (Thompson and Wujek 1997) Trentepohlia were collected on the island of and a need to revise the order (Joubert and Tutuila during this study. The two remaining Rijkenberg 1971; see also Lopez-Bautista et al. genera of the Trentepohliales, Printzina and 2002). Further, variability within and be­ Physolinum, were not found. Algal species tween species is possible due to season and identified and the number of plant hosts exposure (Thompson and Wujek 1997). Spe­ affected by each (in parentheses) were as fol­ cies of Cephaleuros, Phycopeltis, and Stomato­ lows: Cephaleuros expansa Thompson & Wu­ chroon were classified in this study based on jek (7), C. karstenii Schmidle (7), C. minimus recently published keys and descriptions by Karsten (4), C. parasiticus Karsten (19), C. Thompson and Wujek (1997). These char­ virescens Kunze in Fries (115), Phycopeltis epi­ acteristics included morphology and location phyton Millardet (43), P. irreg;ularis (Schmidle) of thalli and sporangiophores, measure­ Wille (1), Stomatochroon coalitum Thompson ments of central filament cells and their & Wujek (1), and S. consociatum Thompson width-to-length ratio, and measurements of & Wujek (4). Specimens collected and not gametangia and sporangia. Specimens are identified to species level included Cephaleuros deposited in the Land Grant , (16), Phycopeltis (4), and Trentepohlia (5). Four American Samoa Community College, Ma­ hosts of C. virescens remain unidentified. laeimi. Hosts with only a few algal thalli were There were similarities and differences accessioned as semipermanent between the five Cephaleuros spp. that aided in slides and photomicrographs. their classification. Thalli of C. expansa, C. 422 PACIFIC SCIENCE· July 2004

FIGURE 1. Subcuticular species of Cephaleuros removed from the upper leaf surface of hosts. A, Filaments of C. expansa fusing to form a false ramulus (branch). B, Irregularly lobed thallus (body) of C. karstenii with multicellular, sterile hairs. C, Entire, closed-ramulate thallus of C. virescens (note sporangiophore [right] with head cell and two sporangiate­ laterals). Scale bars = 25 J.Im.

karstenii, and C. virescens grew beneath the Thalli of C. karstenii and C. virescens were ei­ host cuticle and were more or less circular. ther open- or closed-ramulate (Figure IB,C). The thallus of C. expansa, however, was com­ Ramuli of C. karstenii were four to six fila­ posed of radiating filaments that occasionally ments wide and fan-shaped, and ramuli of crossed each other, or became laterally fused, C. virescens were one to two filaments wide forming narrow, false ramuli (Figure IA). and usually parallel. The width/length ratio Plant-Parasitic Algae in American Samoa . Brooks 423

FIGURE 2. Sporangiophores of two intercellular species of Cephaleuros, with attached host tissue, excised frOID lower leaf surfaces. A, Sporangiophores of C. parasiticus with terminal whorls of sporangiate-laterals. B, Sporangiophores of C. minimus with sporangiate-laterals in twos and threes along one side, and ending in sterile, tapered cells. Scale bars = 25 IlID. of central filament cells was 1: 4 for C. kar­ parastttcus on the same plant), the number stenii and 1:2 for C. virescens. assessed is greater than the total number of and C. minimus plant species collected. Of the infections as­ formed scant, filamentous thalli beneath the sociated with C. virescens 29% (33/112) were cuticle on upper leaf surfaces, grew inter­ moderate and 9% (10/112) were heavy. Only cellularly, and produced sporangiophores nine of the 145 hosts examined had moder­ through lower leaf surfaces. Sporangiophores ate to heavy leaf area covered by the other of C. parasiticus were typical for the genus, Trentepohliales, Phycopeltis, Stomatochroon, composed of a terminal head cell with radiat­ and Trentepohlia. ing sporangiate-laterals (crooked suffultory Of 126 algal infections assessed with the cells and attached zoosporangia) (Figure 2A). necrosis index, no visible tissue death or dis­ Conversely, sporangiophores of C. minimus coloration was caused by Cephaleuros spp. on were unique, with head cells and sporangiate­ 6% (8/126) of the hosts, 39% (48/126) scored laterals along one side and ending in two to 1, 12% (15/126) scored 2, and 43% (54/126) three tapered, sterile, apical cells (Figure 2B). scored 3 (Table 3). The number of algal in­ Trentepohliales were collected from 146 fections assessed with the necrosis index was plant species and cultivars in 101 genera less than either the number of hosts collected and 48 families (Table 1). Ninety percent of or estimates for percentage leaf surface area the hosts (129) were dicotyledonous species. covered, because the necrosis index was ini­ Most algae grew on leaves but were occa­ tiated near the end of the study and some sionally found on stems and . Sapotaceae host specimens were not available for sec­ was the most commonly affected family, with tioning. 14 host species and cultivars. Lichenized thalli of Cephaleuros spp. with Percentage of leaf surface area covered mature perithecia were found on 33 of 124 by Cephaleuros spp. varied by algal and plant hosts and identified as Strigula elegans (c. host species: 66% (109/165) of infections Smith, pers. comm.). Tissue damage caused were light, 25% (42/165) were moderate, and by S. elegans was less severe than (16/33) or 9% (14/165) were heavy (Table 2). Because the same as (17/33) damage caused by the of mixed infections (e.g., C. virescens and C. alga alone. Recording lichenized forms of 424 PACIFIC SCIENCE· July 2004

TABLE 1 A List of Plant Hosts" of CephaleUl"OS, Phycopeltis, and Stomatochroon on Tutuila, American Samoa

Acanthaceae Cupressaceae Aphelandm sinclairiana Nees; Cvir Cupressus sp. L.; Ckar Odontonema tubiftrme (Bertoloni) Kuntze; Cvir Ebenaceae Pseuderanthemum carruthersii var. reticulatum (Seem.) samoensis A. Gray; Pepi Guillaumin; Cvir Euphorbiaceae Agavaceae AleU17tes moluccana (L.) Willd.; Cvir* Cordyline terminalis (L.) Chevallier; Csp Codiaeum variegatum (L.) A. H. L. Jussieu; Cvir*, Pepi Pleomele sp. (Roxburgh) N. E. Brown; Pepi C. v. pictum 'Acubifolium' (L.) A. H. L. Jussieu; Cvir Amaryllidaceae C. v. pictum 'Majesticum' (L.) A. H. L. Jussieu; Cvir*, Crinum asiaticum L.; Cexp Pepi Anacardiaceae C. v. pictum 'Stewartii' (L.) A. H. L. Jussieu; Csp Anacardium occidentale L.; Cvir+ Euphorbia neriiftlia L.; Cvir Mangifem indica L.; Cvir, Cpar*, Scon Flueggea flexuosa Muell. Arg.; Cvir, Pepi Annonaceae Jatropha integerrima Jacquin; Cvir, Pepi muricata L.; Cvir* Pedilanthus tithymaloides L.; Cvir*, Pepi A. muricata 'Cuban Fiberless' L.; Cvir* Fabaceae A. muricata 'Dulce Cuban' L.; Cvir Acacia sp.; Cvir, Csp, Pepi, Scon A. squamosa 'Seedless' L.; Cvir A. mangium Willd.; Csp A. squamosa x A. cherimoya 'Pink Mammoth' L.; Calliandra surinamensis Bentham.; Cvir Cvir*, Cpar* javanica L.; Cvir Rollinia deliciosa Saff.; Cvir+, Pepi, Scoa Intsia bijuga (Colebr.) Kuntze; Ckar, Cvir+, Pepi Apocynaceae Pterocarpus indicus Willd.; Csp Allamanda sp. L.; Cexp Sophora tomentosa L.; Cvir A. cathartica L.; Cvir Heliconiaceae Carissa grandifWra (E. Meyer) A. L. P. P. de Candolle; Heliconia x 'Golden Torch' L.; Cpar Cvir Lauraceae Araceae Persea americana Miller; Cvir Anthurium sp. Linden ex Andre; Cvir, Pepi Leeaceae Epipremnum pinnatum (L.) Engler; Cexp, Cvir* Leea guineensis G. Don; Cexp*, Cpar*, Cvir*, Csp* Araliaceae Loganiaceae Polyscias fruticosa (L.) Harms; Cvir* Fagraea berteroana A. Gray ex Benth.; Cvir P. scutellaria (N. L. Burman) Fosberg; Cvir Lythraceae Arecaceae Cuphea melvilla Lindl.; Cpar*, Csp+, Scon Chrysalidocarpus lutescens H. Wendl.; Pepi Lagerstroemia speciosa (L.) Pers.; Cmin*, Cpar*, Cvir*+, Metroxylon vitiense (H. Wendl.) HookJ.; Cvir, Psp Csp, Scon Pritchardia pacifica Seem. & H. Wendl.; Cvir, Pepi Magnoliaceae Veitchia merrillii (Becc.) H. E. Moore; Cpar*, Pepi Michelia champaca L.; Ckar, Pepi Asclepiadaceae Malvaceae Hoya australis R. Brown; Cvir, Pepi Hibiscus rosa-sinensis L.; Cmin, Cvir, Csp, Pepi Begoniaceae H. tiliaceus L.; Cvir Begonia sp.; Ckar H. tiliaceus cv. L.; Cvir Bignoniaceae Marantaceae Tabebuia heterophylla (DC.) Britton; Cvir Mamnta arundinacea 'Variegata' L.; Cpar*, Cvir, Pepi Bixaceae Meliaceae Bixa orellana L.; Cpar*, Cvir Lansium domesticum Correa; Cvir Bombacaceae Melia azedarach Blanco; Cvir, Psp Cieba pentandra (L.) Gaer01.; Cvir Swietenia macrophylla King; Ckar, Pepi Durio zibethinus Moon; Cvir*, Pepi+ Moraceae Pachira aquatica Aubl.; Cvir Artocarpus altilis (]. D. Hooker) Schlechter; Cvir Burseraceae Ficus benghalensis L.; Cvir Canarium ovatum Engl.; Cvir F. benjamina L.; Cvir* Clusiaceae F. elastica Roxb. ex Hornem.; Cvir Calophyllum inophyllum L.; Cvir+ F. prolixa Forst.f.; Cvir, Pepi C. neo-ebudicum Guillaumin; Pepi F. tinctoria ForstJ.; Cvir Combretaceae Myrtaceae Terminalia samoensis Rechinger; Cvir* Eugenia uniflom L.; Cvir* Convolvulaceae Psidium guajava L.; Cvir*, Pepi Operculina turpethum (L.) Silva Manso; Csp P. guajava 'Waikea' L.; Cpar*, Cvir+ Plant-Parasitic Algae in American Samoa . Brooks 425

TABLE 1 (continued)

Syzygium corynocarpum (A. Gray) C. Mue/I.; Cpar Rutaceae S. inophylloides C. Muell.; Cpar Citrus aurantifolia (L.) Swingle; Cvir S. jambos (L.) Alston; Cvir*, Pepi C. aurantifolia 'Thornless Mexican' L.; Csp Nyctaginaceae Murraya paniculata L. W. Jack; Cvir Bougainvillea spectabilis Willd.; Cvir Sapindaceae Oleaceae Euphoria longan 'Bai Dum' (Lour.) Steud.; Cvir* Jasminum multiflorum (N. L. Burman) Andrews; Cvir, E. longan 'Chompoo' (Lour.) Steud.; Cvir Pepi Litchi chinensis Sonn.; Cvir* J. sambac (L.) Aiton; Cvir Pometia pinnata Forst.; Cvir, Pepi Ligustrum sinense Lour.; Cvir, Pepi Sapotaceae Orchidaceae Chrysophyllum cainito 'Grimal' L.; Cvir+, Pepi Arachnis x maingayi (J. D. Hooker) Schlechter; C. cainito 'Hatian' L.; Cvir, Pepi Cexp*+, Csp*, Pepi+ C. cainito 'Philippine Gold' L.; Cvir Arundina graminifolia (D. Don) Hochreutiner; Cexp*, C. cainito 'Seedless' L.; Ckar* Cpar, Pepi Lucuma mammosum (Jacq.) Merr.; Csp, Pepi+ Spathoglottis plicata Blume; Csp L. nervosa 'Bruce' A. DC.; Csp* Unidentified epiphytic orchid; Pepi Manilkara zapota 'Alano' (L.) D. Royen; Cvir* Unidentified orchid; Cmin, Pepi M. zapota 'Betawi' (L.) D. Royen; Cvir* Oxalidaceae M. zapota 'Ponderosa' (L.) D. Royen; Cpar*, Cvir* Averrhoa carambola 'Jurong' L.; Cvir, Psp Planchonella samoensis H. J. Lam ex Christoph.; Psp A. carambola 'Kajang' L.; Cvir Pouteria sapota (Jacq.) H. Moore & Stearn; Cpar*, A. carambola 'Kembangan' L.; Cvir Cvir+, Pepi Pandanaceae Sandoricum koetjape 'Bangkok' Merrill.; Cpar*, Cvir Pandanus whitmeeanus Mart.; Cvir, Pepi S. koetjape 'Chompoo' Merrill.; Cvir, Pepi Piperaceae Synsepalum dulcificum (Schumach. & Thonn.) W. F. Piper graefJei Warb.; Csp*, Pepi Daniell; Cpar*, Cvir* P. methysticum ForstJ.; Cvir Solanaceae Polygonaceae Brunfelsia americana L.; Cvir* Homalocladium platycladium (F. Von Mueller) L. H. B. pauciflora (Chamisso & Schlechtendal) Bentham; Bailey; Cvir Cvir Rubiaceae Cestrum diurnum L.; Cvir, Pepi, Scon Gardenia jasminoides 'Veitchii' Ellis; Cvir, Csp Sterculiaceae G. taitensis A. L. P. P. de Candolle; Csp Theobroma cacao L.; Cvir, Pepi, Pirr Ixora casei Hance; Cvir Verbenaceae 1. finlaysoniana Wallich ex G. Don; Cexp, Cvir Clerodendrum wallichii Merrill; Cvir, Pepi Morinda citrifolia L.; Cmin* C. x speciosum Van Geert ex Morren.; Cvir Mussaenda erythrophylla 'Rosea' Schumacher; Csp, Congea griffithiana Munir; Cvir Pepi Faradaya amicorum Seem.; Cvir M. frondosa Blanco; Cvir Premna serratifolia L.; Cvir* M. philippica L. C. Richard; Cvir Zingiberaceae Tarenna sambucina (ForstJ.) Durand; Cvir Alpinia purpurata K. Schum.; Ckar

Note: The name of each host is followed by its authority, algal species (Csp, Cephaleuros sp.; Cexp, C. expansa; Ckar, C. kamenii; Cmin, C. minimus; Cpar, C. parasiticus; Cvir, C. virescens; Psp, Phycopeltis sp.; Pepi, P. epiphyton; Pirr, P. i,ngularis; Scoa, Stomatochroon coalitu"'; Scon, S. consociatum), and severity ofdisease (+, >25% of leaf area covered by the alga; *, full-thickness leaf necrosis) caused by Cephaleuros spp. "Table does not include unidentified hosts, except two orchid spp., nor hosts of T,·entepohlia.

the nonparasitic species Phycopeltis and Tren­ plant host range in American Samoa (Table tepohlia was outside the objectives of this 1). Most of the hosts are perennial dicots, study. agreeing with reports from other tropical and subtropical locations (Marlatt and Alfieri 1981, Holcomb 1986, Thompson and Wujek DISCUSSION 1997). However, the number of algal species Algae of the order Trentepohliales, especially identified in American Samoa, especially the C. virescens and P. epiphyton, have a broad five Cephaleuros spp., was higher than re- 426 PACIFIC SCIENCE· July 2004

TABLE 2 of S. consociatum on the underside of leaves Percentage Upper Surface of Plant Host Leaves of the firecracker plant (Cuphea sp.). Water­ Covered by Cephaleuros spp., Tutuila, American Samoa soaking and browning of tissue may occur when sporangiophores of the alga block sto­ No. Hosts Affected at Each mates and inhibit gas exchange (Chapman Level of Leaf Area Covered" and Good 1983, Timpano and Pearlmutter 1983). This incidental damage might not Alga <5% 6-25% >25% qualify Stomatochroon as a plant pathogen, but Cephaleuros expansa 6 it appears to be more than a space opportun­ C. karstenii 7 ist. The autotrophic S. consociatum, for exam­ C. minimus 3 1 ple, was grown on an inorganic salts medium C. parasiticus 12 4 3 C. virescens 69 33 10 by Timpano and Pearlmutter (1983), but all C. sp. 12 4 stages of its life cycle could not be induced. Total 109 42 14 Those researchers suggested that the alga re­

"Some host leaf surfaces were infected by more than one ceives necessary chemicals from its host but species of Cephaleuros. neither benefits nor harms the plant (com­ b No hosts recorded for the algal species at this level. mensalism). McKenzie (1996) was probably correct in suggesting that species of Trentepohliales ported in many areas (Thompson and Wujek collected in American Samoa from mango, 1997). For example, Holcomb (1986) re­ guava, and avocado were Cephaleuros virescens. ported 218 plant hosts in Louisiana but only This was the most commonly identified spe­ one algal species, C. virescens. Marlatt and cies in the current study and the most abun­ Alfieri (1981) did not identify the species of dant alga of the Trentepohliales found on Cephaleuros found on 157 hosts in Florida. these three species. Cephaleuros para­ The only plant damage associated with siticus, Phycopeltis epiphyton, and Stomatochroon Stomatochroon spp. during this study was consociatum were also isolated from these hosts water-soaking caused by a heavy infection (Table 1). Thalli of C. virescens usually grow on up­ per leaf surfaces but were also common on TABLE 3 the undersides of heavily infected leaves. Host Leaf Damage Caused by Cephaleuros spp. on This distribution was especially apparent Tutuila, American Samoa, as Measured by a when leaves were either twisted to expose Necrosis Index" their lower surfaces, had infections along their margins, or were split, with thalli sur­ No. Hosts Affected at Each rounding the break on the upper leaf surface. Level of Necrosisb These conditions favor infection of the lower leaf surface by zoospores swimming in a film Alga o 2 of water connecting the two leaf surfaces Cephaleuros expansa _c 3 4 (Chapman and Good 1983). In a cumulative C. karstenii 4 1 study in Louisiana from 1972 to the mid­ C. minimus 2 2 C. C. parasiticus 14 1980s, Holcomb (1986) reported virescens C. virescens 8 39 15 30 only on upper leaf surfaces of all hosts except C. sp. 4 Camellia japonica, which had thalli on both Total 8 48 15 55 surfaces.

n Necrosis index: 0, no necrosis; 1, superficial necrosis of Stem infections associated with C. virescens the cell layer beneath the thallus, with or without tissue hyper­ were rare in the current study, appearing only plasia; 2, necrosis of >1 cell layer but not full leaf thickness, on kava (Piper methysticum) and the zigzag with or without tissue hyperplasia, erosion, or suberization; 3, full-thickness necrosis from upper to lower leaf surface, or "shot­ plant (Pedilanthus tithymaloides). In the Loui­ hole" symptoms. siana study (Holcomb 1986), however, 17 b Some hosts were infected by more than one species of Cepbaletl1"os. stem infections were reported, and recently

C No hosts recorded for the algal species at this level. workers described cane infections on culti- Plant-Parasitic Algae in American Samoa . Brooks 427

vated blackberry in Arkansas and Louisiana host responses, and leaf spotting, on only 8% (Holcomb et a1. 1998). of 218 hosts. The terms moderately severe Thompson and Wujek (1997) considered and severe were not defined in the Louisiana C. virescens a "relatively innocuous" species, report, however, and may not be comparable causing obvious necrosis on only a few plant with the disease severity scales used in the hosts. They disagreed in general with pub­ current study. lished reports identifying C. virescens as a pri­ Tropical fruit trees in the Sapotaceae were mary agent of disease. Thompson and Wujek more heavily affected by Trentepohliales than attributed the errors in those reports either: other plant families (Table 1). They had (1) to misidentification of the alga, (2) to the broadest host range, a moderate to heavy the alga growing opportunistically in lesions percentage leaf area covered by the algae, and made by other organisms or environmental full-thickness necrosis on many leaves. Most conditions, (3) or to the fungal component of specimens, however, were collected from the lichenized alga being the actual cause of a crowded, poorly maintained fruit the damage. Results of the American Samoa where heavy shading, lack of nutrients, and study differ from those of Thompson and high inoculum levels may have increased host Wujek. Thalli of C. virescens usually occurred susceptibility. Control measures under these in the absence of signs or symptoms of other conditions would include plant spacing and biotic agents or visible damage caused by the thinning to improve aeration and light, opti­ environment. AB algae matured the diameter mum fertilization, orchard sanitation, and se­ of tissue necrosis mirrored thallus growth. lecting cultivars for the local environment. This relationship between the presence of an Algae in the order Trentepohliales re­ algal thallus and host necrosis in the absence main a mystery to most American Samoans, of other lesion-forming organisms suggests because plant-parasitic Cephaleuros species that C. virescens is a primary pathogen, able to do not affect important subsistence crops, cause disease. Until plants can be inoculated such as banana and taro. Occasional blem­ with zoospores of C. virescens and the same ishes caused by algae on other types of pro­ symptoms produced (Koch's postulates), duce and on landscape plants are tolerated. however, its pathogenicity remains tentative Because control measures are not usually ap­ (Agrios 1997). plied and most Trentepohliales have a broad Damage caused by C. virescens on 33 plant host range, their existence in American Sa­ hosts in American Samoa was greater than moa is relatively secure in spite of habitat or equal to damage caused to the same hosts destruction due to population pressure and by its lichenized form, Strigula elegans. This natural disaster. observation argues against Thompson and Wujek's contention (1997) that the fungal ACKNOWLEDGMENTS partner of the lichen is the cause of disease, but agrees with Chapman and Good's find­ My special thanks to D. Wujek for his ing (1983) that necrosis beneath a lichenized continued support, R. Chapman and his lab­ Cephaleuros thallus is produced by the alga oratory for their suggestions and encourage­ before lichenization. Ultrastructural studies ment, and O. C. Steele for assisting in plant have shown that the parasitizes its al­ identifications. gal host and not the plant (Chapman 1976). If a plant- were to associate Literature Cited with C. virescens damage could occur (Chap­ man and Good 1983), but that was not the Agrios, G. N. 1997. Plant . 4th ed. case with S. elegans in this study. Academic Press, New York. Host tissue necrosis was present beneath Chapman, R. L. 1976. Ultrastructure of Cephaleuros thalli on over 90% of the 126 Cephaleuros virescens (Chroolepidaceae; hosts indexed and was moderate to severe on Chlorophyta). 1. Scanning electron mi­ 55% (Table 3). Comparatively, Holcomb croscopy of zoosporangia. Am. J. Bot. (1986) described moderately severe to severe 63:1060-1070. 428 PACIFIC SCIENCE· July 2004

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