Mycologia
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DOI: 10.3852/mycologia.97.4.908
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Mycologia, 97(4), 2005, pp. 908-913.
© 2005 by The Mycological Society of America

New species of Septobasidium from southern Costa Rica and the southeastern United States


Daniel A. Henk 1

     Department of Biology, Duke University, CB 90338, Durham, North Carolina 27708

   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 

New species are described in Septobasidium, a genus of urediniomycete parasites on scale insects. One new species, S. gomezii, is described from Costa Rica, and another, S. meredithiae, is described from Louisiana. S. gomezii is most similar to S. septobasidioides, but macroscopic and microscopic differences support it being a distinct species. S. meredithiae is similar to S. alni and S. castaneum but differs from these species in several macroscopic and microscopic characters, especially when the species are observed on the same host tree and insect species. Another species collected only once in Costa Rica is listed with observations but it is not formally described here. This Septobasidium species shares some key characteristics with S. ramorum but combines a dense, compact, nearly black thallus and pigmented probasidia-like structures with spindle-shaped haustoria. Implications for taxonomy, morphological evolution and host specificity in Septobasidium are discussed.

Key words: coccoidea, gomezii, Melanaspis, meredithiae, urediniomycetidae


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Fungi in the genus Septobasidium live symbiotically with scale insects (Coccoidea) and form a complex relationship that is parasitic on individual insects but may be mutualistic from the perspective of a population of insects (Couch 1938Go). The genus contains more than 175 described species and is in the subclass Urediniomycetidae (Swann 2001Go). Septobasidium species commonly are found on the branches and leaves of trees and shrubs and rarely on the fruit or roots of trees and shrubs. Fruit bodies generally are perennial and form roughly circular patches that vary in diameter from 1 mm to more than 25 cm. Species vary in thickness from less than 1mm to several centimeters, and consequently some smaller, thinner Septobasidium species are difficult to detect in the field and usually are found only because they occur together with larger, more obvious species on trees infested with suitable scale insects. Within the genus there is considerable variation in discrete microscopic and macromorphological characteristics. Species may differ in haustorial shape, the number of cells per basidium, persistence of a probasidium, presence of pillars, number of mycelial layers in a colony or color of a colony, for example. Usually any particular combination of these discrete characters has defined a species, with relatively little emphasis placed on continuously variable characters such as spore size or colony diameter. Taxonomic knowledge of Septobasidium is derived almost entirely from the work of J.N. Couch, in particular his book "The Genus Septobasidium" (1938). In that book, previous articles and a later publication, Couch described numerous species of Septobasidium, finding abundant material and morphological variation in the tropical and temperate regions to which he had access (Couch 1929Go, 1935Go, 1938Go, 1946Go).

A current study to examine the ecology and evolution of Septobasidium has been undertaken, and as part of that study numerous species were collected in Costa Rica and the southeastern United States. Among them are three new species described here.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Collecting expeditions were conducted in 2000–2003. When possible, sections of hymenium were suspended above yeast malt peptone agar (YMA) allowing basidiospores to be discharged onto the agar surface. Isolates derived from single basidiospores were made by transferring cells from isolated yeast colonies after basidiospore germination. All cultures have been deposited in the ARS entomopathogenic fungus collection (ARSEF). Freshly collected and dried specimens were studied with Zeiss and Leitz light microscopes. Squash mounts were prepared in 3% KOH, tap water or glycerol. Small tissue samples were embedded in Fisher Histo-Prep frozen tissue media and sectioned using a Tissue-Tek II Cryostat microtome then mounted in glycerol. Color names and numbers are from Smithe (1975)Go.


   TAXONOMY
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 TAXONOMY
DISCUSSION
 LITERATURE CITED
 
Septobasidium gomezii D.A. Henk sp. nov. FIGS. 1Go–2Go



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  		FIG. 1. Septobasidium gomezii. Bar = 1 cm.

 


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  		FIG. 2. Microstructure of S. gomezii. A. Cross section of the part of the fungus around an insect showing insect house structure with dome (1) and pillars (2) supporting a "roof" over which the upper layer forms. The upper and bottom layers (3 and 4) extend to the rest of the fungus, while the domes, pillars and "roof" of the middle layer are formed only around insects, creating two distinct forms in cross section depending upon the presence of insects in that area. B. Immature basidia, basidia and spore C. Irregularly coiled haustoria. Bars: A = 50 µm, B = 10 µm, C = 10 µm.

 
Basidoma resupinatum, brunneolus, e partibus duabus compositum. Pars prima 80–150 µm crassa e subiculo et strato supero. Subiculum atrobrunneum, 10–25 µm crassum ex hyphis bruneis, 3.5–5 µm latis. Stratum superum fertile, cinnamomeum, 30–90 µm crassum, faciliter separabilis. Hymenium 20–50 crassum e hyphis hyalinus, 2.5–3.5 µm latis et basidia. Immatura basidia sublobosa, 9–12 µm lata, hyalina, non persistentia. Metabasidia cylindrical, recta, 9–12 µm x 38–48 µm, transverse septata 4-cellata. Sterigmata 11.5 x 14.3 µm. Basidiosporae elipticae, curvatae, 6.3–7 x 15–20 µm. Pars segunda circa insecta e subiculo et strato superum et strato medium columnatum. Columnae circa insecta, 200–300 µm altae ex hyphis atrobrunneis, Contextum insidens columis 80–100 µm crassum ex hyphis atrobunneis intracatis textum.

Fruit bodies are resupinate, forming felt-textured, irregularly shaped patches that may extend tens of centimeters and are composed of two mature parts. One part has just two main horizontal layers and makes up most of the fungal thallus, while the other is just formed around insects and forms another layer with columns in addition to the layers present elsewhere. The first part is 80–150 µm thick and has two layers, (i) subiculum and (ii) upper. The subiculum is dark brown (219a), thin (10–25 µm) and composed of thick brown hyphae, 3.5–5 µm diam, that extend over the bark enveloping almost anything else on the surface of the plant. The upper layer is light brown (219c) 30–90 µm thick and is where the fertile part of the fungus is formed. This layer is fragile, easily separated from the lower layers and may extend to cover anything protruding above the plant surface. On the surface of the upper layer the immature basidia, basidia and branched hyaline hyphae form and pile up to 50 µm thick, giving the fertile parts of the fungus a pulverulent appearance. The auricularioid basidium elongates and is divided transversely by three septa to form a four-celled basidium 9–12 x 38–48 µm. Bent elliptical basidiospores (6.3–7 x 15–20 µm) are formed from the 11.5–14.3 µm long sterigmata. Around scale insects, the fungus forms a distinct second part of the thallus including a middle pillared layer between the subiculum and upper layer present elsewhere in the fungus. In this second part, pillars arise from the subiculum in roughly circular patches of closely adherent thick hyphae, 4–5.3 µm diam, that angle away from the surface toward a central point, forming an open dome 130–180 µm tall. The open dome is formed only over a scale insect infected by coiled hyphae 3–4.5 µm diam. From the periphery of these thicker patches arise black thick ropey pillars, 200–300 µm high. Hyphae spread between and around the pillars above the partially enclosed insects to form a distinct dark covering 80–100 µm thick. Sometimes the pillars may continue through the "roof." The upper layer forms over the "roof."

Etymology.— – In recognition of the assistance of Luis Diego Gomez, Costa Rican naturalist and director of the Las Cruces Biological Research Station.

Specimens examined.— – COSTA RICA. COTO BRUS: Las Alturas Biological Research Station 21 June 2000 DAH051 (31) (HOLOTYPE DUKE, ISOTYPE UCR); Las Cruces Biological Research Station 22 June 2000 DAH046 (27a), DAH047 (27b).

Commentary.— – S. gomezii is most similar to S. septobasidoides. Both infect Epidiaspis scale insects and have been collected from Costa Rica. These two species also share the distinctive "insect house" structure associated with scale insects and share most of their microscopic characteristics. However S. septobasidioides has primarily S-shape spores that are less frequently observed in S. gomezii. Further S. gomezii is easily distinguishable from S. septobasidioides by the latter’s gray color and by the lack of pillars in S. gomezii except where associated with scale insects while Septobasidium septobasidioides forms pillars throughout. S. septobasidioides also has a distinctly papery upper layer that sometimes rolls upward in the marginal region, while S. gomezii has a more closely attached but fragile upper layer that is not papery and does not roll upward.

Septobasidium meredithiae D.A. Henk sp. nov. FIGS. 3Go–4Go



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  		FIG. 3. Septobasidium meredithiae Bar = 1 cm.

 


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  		FIG. 4. Microstructures of S. meredithiae. A. Cross section showing subiculum with pillars supporting the upper layer. B. Empty probasidial cells with basidia and spores. C. Irregularly coiled haustoria. Bars: A = 50 µm, B = 10 µm, C = 10 µm.

 
Basidioma resupinatum, hepaticum, 250–400 µm crassum e partibus tribus stratosa. Subiculum hepaticum, distinctum, 25–50 µm crassum e hyphis brunneis, 3–4.3 µm latis. Stratum medium columnatum. Columnae 70–125 µm altis, 60–100 µm crassum e hyphis 3.8–5 µm latis. Stratum superum 200–250 µm crassum, pulverulentum, non papyraceum, leviter tenax. Probasidia hyalina, persistentia, globosa 9–13 µm diametro. Basidia cylindrica, recta, 5–6.25 x 42.5–50 µm, transverse septata, 4-cellulata. Sterigmata 2–2.5 x 5.5–6.7 µm. Basidiosporae 3.5–4 x 11.25–13.5 µm.

Fruit body is resupinate and brown tinged with yellow (199B). The thallus is 250–400 µm thick and divided into three concolorous layers. The subiculum is 25–50 µm thick and composed of hyphae that are 3–4.3 µm wide. The middle layer is composed of hyphae 3.8–5 µm wide that twist together to form short pillars 70–125 µm high and 60–100 µm wide. The top layer is slightly tough, not papery, and pulverulent on the surface. Probasidia are persistent and not pigmented. They are globose and 9–13 µm diam. The probasidia empty into straight, 4-celled, transversely septate, cylindrical basidia 5–6.25 x 42.5–50 µm. Elliptical to bent elliptical basidiospores 3.5–4 x 11.25–13.5 µm are borne on sterigmata 2–2.5 x 5.5–6.7 µm. Coiled haustoria fill Diaspidiotus liquidambaris insects but form a dense cluster of straight hyphae exiting insects at the vulva. Basidiospores bud and readily form yeast colonies on YMA.

Etymology.— – In recognition of the guidance provided by Meredith Blackwell, mycologist and Boyd Professor at Louisiana State University.

Specimens examined.— – USA. LOUISIANA: Tangipahoa Parish, Sandy Hollow Wildlife Management Area 17 May 2003 DAH 257 (HOLOTYPE DUKE); Washington Parish, Bens Creek Wildlife Management Area 17 May 2003 DAH263, DAH264 (culture available).

Commentary.— – S. meredithiae is similar to several common species, especially S. alni and S. castaneum with which it often occurs on the same host plant. However S. meredithiae is easily distinguished from these other species in the field by its color and distinct upper layer and by its smaller thinner-walled probasidia. S. alni is variable in color but generally lacks the yellowish tints of S. meredithiae, and S. alni on Liquidambar has distinctly flaky, papery and smooth upper layer nearer to fawn (25), sometimes with a purplish tint. The probasidia of S. alni also form inside the empty walls of previous probasidia, a characteristic not shared with the smaller more consistently globose probasidia of S. meredithiae. S. castaneum has a smooth, shiny upper layer and has less distinct pillars that are considerably taller and branching. S. meredithiae is apparently specific to Diaspidiotus liqudiambaris while S. alni and S. castaneum are host generalists, infecting insects from both the Aspidiotini and Diaspidiotini.

Septobasidium sp. FIGS. 5Go–6Go



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  		FIG. 5. Septobasidium sp. The fungus is cryptic due to the coverage of liverworts, and in this photo it is enveloping the branches such that it appears only as a dark, indistinct, tough mycelial mat. Bar = 1 cm.

 


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  		FIG. 6. Microstructure of Septobasidium sp. A. Cross section of thallus showing dense context slightly looser at the surface. B. Punctate probasidia like structures C. Spindle-shape haustoria. Bars: A = 50 µm, B = 10 µm, C = 10 µm.

 
Fruit bodies are resupinate and dark brown to nearly black (119). They are 300–500 µm thick, fairly dense and composed of two layers. The subiculum is relatively indistinct and partly interwoven with the cortical layers of the plant. The hyphae of the subiculum are deeply brown, 4.5–6 µm thick and woven together to form a context. The top layer is composed of thinner hyphae, 2.5–3.5 µm, and dotted with darkly pigmented globose probasidia. The probasidia-like structures are 14–16.3 µm wide with thick punctate walls. Haustoria formed inside the bodies of infected insects, Melanaspis tenebricosa, are spindle shape.

Specimen examined.— – COSTA RICA. COTO BRUS: Las Alturas Biological Research Station 21 June 2000 DAH 045 (26).

Commentary.— – This species most closely resembles S. ramorum (commonly but incorrectly called S. curtisii, see Gomez and Henk 2004Go) in its blackish, dense macromorphology and presence of thick-walled, ornamented and darkly colored probasidia. However the present species lacks the pillars or spines that S. ramorum forms, and the present species forms spindle-shape haustoria rather than the irregular coils that S. ramorum forms inside infected scale insects. S. fumigatum forms spindle-shape haustoria and is the only other species known to infect Melanaspis tenebricosa. However, S. fumigatum is smoke gray, has a much more fragile texture and lacks dark thick-walled probasidia. The probasidium-like structures might not be probasidia, and their presence in areas other than the upper surface suggest that thay might not function as reproductive structures. However the thick, ornamented wall of these nearly spherical cells does not have any analogous structure in another species of Septobasidium and they are of the appropriate size for basidium development in other species. Finally, the present species does not closely resemble any of the other Septobasidium species for which basidia have not been observed.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 TAXONOMY
 DISCUSSION
LITERATURE CITED
 
These three newly described species do not expand the overall morphological boundaries of Septobasidium but instead serve to highlight the "mix and match" morphological variability in the genus. S. gomezii combines the formerly unique "insect house" structure of S. septobasidioides with a different color common to other species of Septobasidium. Unlike S. septobasidioides, S. gomezii lacks pillars except around insects, and this phenomenon is also similar to patterns of pillar and spine formation in species such as S. ramorum and S. apiculatum. The undescribed species form Costa Rica combines a nearly black fruit body and the thick darkened ornamented probasidia similar to species such as S. ramorum with the spindle-shape haustoria present in other species including those that infect Melanaspis insects. S. meredithiae is similar to the common Septobasidium morphology found in S. alni, S. carestianum, S. cavarae, S. castaneum and many others. These species all are similar, differing mostly in color and pattern of growth, which may be particular to a host. Although he expressed skepticism regarding the uniqueness of many of these species, Couch did recognize them. As molecular studies progress, the correctness of these morphologically similar species undoubtedly will be tested, as will the phylogenetic functionality of any of the apparently "mix and match" characters primarily used in descriptions of Septobasidium species, and the relationship between host generalist species and morphologically similar host specialists.

It is a testament to the completeness of Couch’s work that, to my knowledge, only a single species, S. wilsonianum (Gomez and Kisimova-Horowitz 2001), has been newly described since Couch’s final species descriptions in 1946. However it is also an indicator of the lack of attention that this locally common and perennial genus receives from mycologists. Approaching identification and taxonomy within any fungal genus can be daunting, but Septobasidium has a tremendous advantage over many fungal taxa in that there is currently one complete source for almost all of the taxonomy, descriptions, illustrations and photographs. This enables even the novice collector to gather the literature needed for species identification rapidly.


   ACKNOWLEDGMENTS
 
I am grateful to Luis Diego Gomez and Meredith Blackwell for letting me use their names and for providing their helpful advice, guidance, enthusiasm and mycological expertise. I thank Rebecca Yahr, Carla Rydholm, Tim James, Jeri Parrent, Cindy Henk and two anonymous reviewers for helpful comments related to this manuscript; Cecile Gueidan for assistance in preparing sections and Bill Burk for help with herbarium material and literature. I also thank these people for their assistance and support of field collecting and culturing: Rytas Vilgalys, Shannon Henk, Juan Luis Mata, William Henk and Sung-Oui Suh. This research was supported by Andrew W. Mellon Foundation fellowships from the Organization for Tropical Studies and Duke University.


   FOOTNOTES
 
Accepted for publication March 28, 2005.

1 E-mail: dah{at}duke.edu


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 TAXONOMY
 DISCUSSION
 LITERATURE CITED
 
Couch JN. 1946. Two species of Septobasidium from Mexico with unusual insect houses. J. Elisha Mitchell Sci Soc 62:87–94.

———. 1935. Septobasidium in the United States. J. Elisha Mitchell Sci Soc 51:1–77 and 44 plates.

———. 1929. A monograph of Septobasidium. Part I. Jamaican species. J. Elisha Mitchell Sci Soc 44:242–260.

———. 1938. The Genus Septobasidium. University of North Carolina Press, Chapel Hill. ix, 480 p.

Gómez, LD, Kisimova-Horovitz L. 2001. A new species of Septobasidium from Costa Rica. Mycotaxon 80:255–259.

———, Henk D.A.. 2004. Validation of the species of Septobasidium (Basidiomycetes) described by John N. Couch. Lankesteriana 4:75–96.

Smithe FB. 1975, Naturalist’s Color Guide: American Museum of Natural History, New York, New York, USA.

Swann EC, Frieders EM, McLaughlin DJ. 2001. Urediniomycetes. In: McLaughlin DJ, McLaughlin EG, Lemke PA, eds. The Mycota Vol VII, Systematics and Evolution, Springer-Verlag, Berlin, p 37–56.




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