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Scleroderma stellatum versus Scleroderma bermudense: the status of Scleroderma echinatum and the first record of Veligaster nitidum from the Virgin Islands

     Instituto de Ecología, Apartado Postal 63, Jalapa, Ver. 91070, Mexico

Orson K. Miller, Jr.

     P.O. Box 858, McCall, Idaho 83638

D. Jean Lodge

     Center for Forest Mycology Research, U.S. Department of Agriculture, Forest Service, Forest Products Lab., P.O. Box 1377 Luquillo, Puerto Rico 00773-1377

Timothy J. Baroni

     Department of Biological Sciences, State University of New York College at Cortland, Cortland, New York 13045-0900

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS LITERATURE CITED

 

The type of Scleroderma stellatum from Brazil exhibits a sharp echinulate, dark brown peridium, and the type of S. bermudense from Bermuda has a peridium that is loosely woven and fibrillose, whitish to pale brownish. These characters indicate two independent species. This information is contrary to that of Guzmán in 1970, who interpreted S. bermudense to be a synonym of S. stellatum based on the similar spores. Scleroderma echinatum from Borneo and Panama, as recently discussed by Guzmán and Ovrebo, also has an echinulate, dark brown peridium and is a synonym of S. stellatum. All these fungi have a stellate dehiscence. New records of S. bermudense from the Greater Antilles and Mexico’s Pacific Coast, and Veligaster nitidum from Virgin Islands also are discussed.

Key words: Gasteromycetes, new records, Scleroderma, Sclerodermataceae, tropical fungi, Veligaster

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS LITERATURE CITED

 
Recent information and new material on Scleroderma species with stellate dehiscence gathered by Reid (1977) in Trinidad, new collections by the senior author from the Pacific Coast of Mexico, new collections by Miller and Lodge in the Greater Antilles including Puerto Rico, the Dominican Republic and Virgin Islands, and additional collections by Ovrebo from Panama moved the authors to re-examine and revise the status of S. bermudense Coker and S. stellatum Berk. The senior author first considered S. bermudense to be a synonym of S. stellatum based on the stellate dehiscence and similar structure of the spores in both fungi (Guzmán 1970). However, a restudy of the poorly preserved holotype of S. stellatum showed it possessed an echinulate, chocolate-brown peridi-um, unlike S. bermudense, which has a loosely woven and pale peridium. In addition, S. echinatum (Petri) Guzmán, recently studied by Guzmán and Ovrebo (2000) from Panama, has the same peridium characters as those observed in S. stellatum.

This paper presents a revised concept for S. stellatum and its synonymy with S. echinatum, while removing it from synonymy with S. bermudense, which we now consider to be an independent species. The distribution of S. bermudense is expanded, and its close association with Coccoloba uvifera (L.) Jacqu., a putative ectomycorrhizal associate, also is reported. Last, Veligaster nitidum (Berk.) Guzmán & Tapia is reported for the first time from the Virgin Islands in the Greater Antilles.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS LITERATURE CITED

 
Macro- and microscopic studies of the types of Scleroderma stellatum and S. bermudense, as well as recent collections from Bermuda, Panama, Puerto Rico, the Dominican Republic, Virgin Islands and Mexico, are the basis of this work. Microscopic observations were made from rehydrated sections of basidiomata mounted in 5% KOH, in lactophenol, or in 1% Congo Red mixed on the slide with a drop of 5% KOH. Color comparisons were made using the plates of Kornerup and Wanscher (1967) (e.g., 12F2-3).

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS LITERATURE CITED

 
Scleroderma stellatum Berk. in Hooker’s J & Kew Gard Misc 8:278, 1856. FIGS. 1–10 and 24

View larger version (51K): [in this window] [in a new window]   FIGS. 1–4. Scleroderma stellatum. 1. Basidiome (reconstructed). 2. Scale of the exoperidium. 3. Spores. 4. Hyphae and cells of the exoperidium base (all from the holotype). Scale bar: FIG. 1 = 10 mm, FIGS. 2–4 = 10 µm.

View larger version (41K): [in this window] [in a new window]   FIGS. 5–12. Scleroderma stellatum and S. bermudense. 5–10. S. stellatum, 5. Mesoperidium. 6. Endoperidium. 7. Scale of the exoperidium. 8. Spores. 9. Basidiomata (young and mature). 10. Scales of the peridium (FIGS. 5–6 from the type; FIGS. 7–10 from Vitter 5717 first considered S. echinatum). 11–12, S. bermudense, 11. Spores. 12. Tramal hyphae in the gleba (Guzmán 32973). Scale bar FIGS. 5–8 and 11–12 = 10 µm; FIG. 9 = 10 mm; FIG. 10 = 3 mm.

View larger version (106K): [in this window] [in a new window]   FIG. 24–25. Scanning microscopy of the spores of Scleroderma stellatum (24) and S. bermudense (25) (24 holotype, 25 Baroni 9814). Scale bar = 1 µm in FIG. 24, 2.5 µm in FIG. 25.

= Caloderma petrianum E. Fischer, in Engler & Prantl, Natürl Pflanzenfam 7a, 2, p. 38, 1933 (!).

= Scleroderma echinatum (Petri) Guzmán, Ciencia 25: 200, 1967 (!).

=? S. violaceum Lloyd, Myc Writ 7:1306, 1924.

=? Sclerangium brasiliense P. Henn., Hedwigia 43:154: 1904.

non S. stellatum Berk. sensu Guzmán, Darwiniana 16:310, 1970.

non S. bermudense Coker, Mycologia 31:624, 1939 (see below).

non Caloderma echinatum (Sacc. & Paoletti) E. Fischer, in Engler & Prantl, Natürl Pflanzenfam 7a, 2, p. 38, 1933 (Tuber echinatum Sacc. & Paoletti, Atti R Inst Veneto Sc Lett Art 6, ser 6:27, 1888; Neo-saccardia echinata [Sacc. & Paoletti] Mattirolo, Atti R Acc Sc Torino 56:27, 1921).

Basidiomata (FIGS. 1 and 9) globose or subglobose, sessile or very shortly stipitate, up to 45 mm diam, with a thin peridium up to 0.5 mm thick, elastic and brittle in dried specimens, reddish brown to very dark brown, hardly echinulate, with thick, pyramidal scales or spines, up to 1.5 mm high above and shorter near the base (FIGS. 9–10), and which are acute or stellate when mature, base of the peridium pale, smooth or covered by short, mustard-yellow filaments (FIG. 1). Dehiscence by irregular or torn tear, open stellately in holotype and Ovrebo 4049, or sometimes by an apical irregular pore (Vitter 5117). Gleba fleshy when young (in material from Panama), subareolate in holotype and other collections, dark purple to brownish violet, with white, thin, irregular filaments, powdery with age, dark brownish violet, with a few irregular white filaments, which eventually disappear. Spores (5–)6–7(–9) µm diam (FIGS. 3, 8 and 24), including the spines, which are up to 1.5 µm long, forming a subreticulum, although the young spores are without a reticulum. Exoperidium formed by fascicles of erect hyphae (FIGS. 2, 4 and 7), thick-walled (up to 6 µm thick), yellowish brown or reddish brown, 38–130 x 7–35 µm, smooth or encrusted, apex obtuse or acute, sometimes capitate. Mesoperidium (FIG. 5) subcellular, with globose elements, up to 35 µm diam, thick-walled, walls up to 3 µm thick, hyaline (yellowish in mass), mixed with long, hyaline hyphae, 4–20 µm wide. Endoperidium (FIG. 6) thin and formed by hyaline, thin-walled hyphae, 4–20 µm wide, surrounding the gleba. The filaments at the base of the exoperidium (FIG. 4) are formed by thick-walled, cylindric or sublageniform elements, 5–10(–20) µm wide, with brownish yellow walls, up to 2 µm diam arising from prostrate, branched, hyaline hyphae, 2.5–18 µm wide, thin to thick-walled, smooth, with brown encrustations.

Habitat and distribution. – Solitary or gregarious on soil, in tropical rain forests. Patouillard and Gaillard (1888) reported it on an ant nest. It is known from Brazil (Berkeley 1856, Berkeley and Cooke 1877), Venezuela (Dennis 1970, Patouillard and Gaillard 1888), Panama (Garner 1956, Guzmán and Ovrebo 2000), Borneo (Petri 1900).

Specimens examined. – VENEZUELA, Amazonia, Panuré, 1884, Spruce ? (holotype K[M]105766). PANAMA, San Blas, Port Obaldia, Sep 1911, Vitter 5717 (BPI); Panama Canal Zone, Barro Colorado Island, 12 Jul 1925, Dodge (BPI); Miller Trail, 11 Aug 1997, Ovrebo 3603; 14 Aug 1997, Ovrebo 3638; Latham Trail, 7 Aug, 2001, Ovrebo 4049 (all of them in SCZ and XAL, except the last, which is in SCZ).

Comments. – Scleroderma stellatum, described by Berkeley (1856) from Panuré, Venezuela, was considered by Guzmán (1970) to possess an off-whitish to straw-colored, smooth or somewhat scaly peridium. With this concept, Guzmán (1970) considered S. bermudense to be a synonym of S. stellatum, which has the same type of spores and stelliform dehiscence. However, a recent restudy of the type by Guzmán and Ramírez-Guillén, confirmed by Lodge, revealed that the peridium has acute brown scales, formed by thick-walled, dark brown, raised hyphae, resembling those observed by Guzmán (1970) and Guzmán and Ovrebo (2000) in collections of S. echinatum from Panama. Berkeley’s (1856) original description of the peridium was: "rough with minute, stellate warts." The description of Caloderma echinatum by Petri (1900) and C. petrianum by Fischer (1933) agrees with the type of Scleroderma stellatum. The fungus described by Saccardo and Paoletti as Tuber echinatum from Malaysia in 1888, and considered by Mattirolo (1921) as Neo-saccardia echinata, and by Fischer (1933) as Caloderma echinata, appears to be another species of Scleroderma, close to S. echinatum. The type of Caloderma echinata unfortunately appears to be lost (Guzmán 1970). Neo-saccardia echinata has large spores, 10–12 µm diam not including the spines (Mattirolo 1921). The synonymy of Caloderma Petri (1900) with Scleroderma follows the concept of Guzmán (1970), based on the absence of a true capillitium and the development of the spores after they are expelled from the basidia and surrounding by cells (known as "nurse cells") of the collapsed trama. This concept first was presented by Clements and Shear (1957). Scleroderma stellatum s. Patouillard & Gaill. reported from Venezuela by Dennis (1970) seems to belongs to S. stellatum s.s.

Guzmán and Ovrebo (2000) classified S. echinatum in the new section Caloderma Guzmán & Ovrebo of the genus Scleroderma. This was based on the structure of the echinulated peridium, formed by thick-walled, brown hyphae, not seen in other species of Scleroderma.

The probable synonymy of S. violaceum Lloyd and S. stellatum, described by Lloyd in 1924 (Lloyd 1898–1926) from the Congo and considered doubtful by Guzmán (1970), is based on the study of the poorly preserved type: Lloyd 24888 at BPI. The material has a thick, dark-brown peridium and seems to have minute warts. The spores are similar to those found in S. stellatum. Another probable synonym of S. stellatum is Sclerangium brasiliense P. Henn., described from Amazonia in Brazil (Hennings 1904). The type appears to be lost (Guzmán 1970), but the description of the fungus indicates the peridium was "rufobrunneo squamoso" and thick with a stellate dehiscence.

Scleroderma bermudense Coker. Mycologia 31:624, 1939. FIGS. 11–22 and 25

View larger version (131K): [in this window] [in a new window]   FIGS. 20–22. Basidiomata of Scleroderma bermudense (FIG. 20 from Miller 27349. FIG. 21 from Miller 27237. FIG. 22 from Miller 27245). Scale bar = 5 mm.

= Sclerangium bermudense var. trinitensis Reid, Kew Bull 31:681, 1977.

Basidiomata globose to subglobose, 18–34 mm wide, smooth or with shallow depressions over the surface, dingy white or tinted gray, with gray to brown rhizomorphs and loose arachnoid hyphae and clinging sand over the surface (FIGS. 20–22). Dehiscent at maturity, splitting to form a roughly stellate pattern (FIG. 20) of 4–6 rays. Gleba firm, subareolate, with white filaments, deep purple (12F2-3 to 14F4-5), light purple (12B3-4) to dull grayish purple (10E2-3) with age. Peridium 2.5–3 mm thick, 1–1.5 mm when dry, surface whitish to pale brown, or pale gray, formed by loosely woven fibrils. Context yellowish brown or with a light pink tint. Peridium is formed by three layers: exoperidium, mesoperidium and endoperidium. The first (FIGS. 13 and 18) is formed by hyaline, prostrate to suberect or mixed hyphae, 2–6 µm wide, sometimes with 10 or more hyphae in fascicles, up to 70 µm high, thin- to thick-walled, walls up to 1.5 µm thick; hyphae smooth or lightly encrusted, with the apex obtuse or rostrate. The mesoperidium (FIGS. 14 and 16) is formed by hyaline, thin- or thick-walled hyphae, sometimes inflated, 3.5–20(–26) µm wide. The endoperidium (FIGS. 15 and 17) is formed by thin- to thick-walled hyphae, 3–7 µm wide, that forms a thin cottony membrane surrounding the gle-ba. This is not a true endoperidial layer, as observed in other gasteromycetes (e.g., Geastrum), because it is a thin (<0.1 mm thick), ephemeral layer, that disappears when the basidiome opens by the dehiscence. Spores globose, 5–7(–10) µm diam, including the spines, which are 0.4–1 µm long, forming a partial reticulum at maturity (FIGS. 11 and 19); surrounding by hyaline, thin- or thick-walled tramal hyphae, with clamp connections and "nurse cells" (FIGS. 12, 19 and 25).

View larger version (36K): [in this window] [in a new window]   FIGS. 13–15. Scleroderma bermudense. 13. Exoperidium. 14. Mesoperidium. 15. Endoperidium (Miller 27245). Scale bar = 10 µm.

View larger version (32K): [in this window] [in a new window]   FIGS. 16–18. Scleroderma bermudense. 16. Mesoperidium. 17. Endoperidium. 18. Exoperidium (FIGS. 16–17 from Miller 27245, FIG. 18 from Guzmán 21087). Scale bar = 10 µm.

View larger version (117K): [in this window] [in a new window]   FIG. 19. Scleroderma bermudense, basidiospores (note the collapsed hyphae of the trama and the "nurse cells") (Guzmán 32937). Scale bar = 10 µm.

Specimens examined. – BERMUDA ISLANDS, Grape Bay, 29 Nov 1938, Seaver & Waterston 15A (holotype, NY); 27 Nov 1940, Seaver & Waterston 336 (NY); Elbow Beach, 4 Dec 1938, Seaver & Waterston 119 (NY); 11 Dec 1938, Seaver & Waterston 183 (MICH; NY); Whetzel (NY). BAHAMAS, Long Cay, Brace 4226 (NY); Britton (NY). PUERTO RICO, Jan 1923, Seaver & Chardon 128 (NY); Seaver & Chardon 503 (NY); Guanica, 1915, Britton 4922 (NY); near Loiza, Piñones Beach, 19 Nov 1996, Baroni 8350 (CORT); 27 Feb. 2004, Baroni 9814, comm. Lodge (CORT); 14 Jan 1998, Miller 27237; 27244; 27245; 27249; 27250 (all in VPI). Mona Island Commonwealth Reserve, Sardinera, 24 Sept. 1995, Nieves-Rivera PR-54 (IA; VPI); 24 Sep 1995, Nieves-Rivera PR-269 (MAPR; VPI); 25 Sep 1995, Nieves-Rivera PR-275 (UPRRP; VPI); 26 Sep 1995, Nieves-Rivera PR-193 (NY; VPI). BARBADOS, 24 Jun 1905, Lewton (Lloyd 9123, BPI); Freeman (Lloyd 9128, BPI). VIRGIN ISLANDS, Guana Island, White Bay Beach, 11 Oct 1998, Clum G-58 (GUA 203); 19 Oct 1997, Lodge G-74 (GUA 162); 3 Oct 1998, Lodge & Clum G-22 (GUA 207). BRITISH VIRGIN ISLANDS, Guana Island, White Bay Beach, 19 Oct 1997, Lodge (GUA-162; CFMR; K); 3 Oct 1998, Lodge & Clum (GUA-207; CFMR); 11 Oct 1998, Clum (GUA-203; CFMR). CUBA, Wright 895 (NY as Stella americana). DOMINICAN REPUBLIC, Prov. Higuey, Punta Cana Beach Resort, 16 Jul 2001, Lodge DR-2100 ( JBSD). U.S.A., FLORIDA, Mathemon Hammock, Sep 1942, Singer F-801 (NY, F as S. cepa ?); Miami, Singer F-680 (F as S. cepa ?). MEXICO, Quintana Roo, N of Puerto Morelos, 13 Nov 1981, Guzmán 21096 (XAL); S of Tulum, 1 Nov 1984, Chacón 2755 (XAL); near Cancun, 2 Nov 1984, Guzmán 24785 (XAL); Yucatan, Dzilam to Telchac, near Chabian, 28 Oct 1984, Guzmán 24742 (XAL); near Telchac, 5 Aug 1983, Guzmán 23624 (XAL). GUERRERO, Ixtapa-Zihuatanejo, 16 Jun 1999, Guzmán 32973 (XAL).

Comments. – Scleroderma bermudense is characterized by the structure and the stellate dehiscence of its peridium, subreticulate spores, absence of capillitium and the thin and ephimerous endoperidium, as in all the species of section Sclerangium Guzmán, where S. bermudense belongs, according to Guzmán (1967, 1970). The tramal hyphae were considered by Reid (1977) as capillitium, but following Guzmán (1970) the true capillitium is absent in Sclerodermataceae. These tramal hyphae are really the generative hyphae in the young trama of the gleba, which collapse and produce the typical "nurse cells" that surround the young spores. Sclerangium bermudense var. trinitensis by Reid (1977) is considered a synonym of the typical variety, because it was based only on the inflated mesoperidium elements, up to 26 µm wide.

Veligaster nitidum (Berk) Guzmán & Tapia. Doc Mycol 25 (98–100):188, 1995. FIG. 23

View larger version (133K): [in this window] [in a new window]   FIG. 23. Veligaster nitidum (Lodge G-167). Natural size.

= Scleroderma tenerum Berk. & M. A. Curtis, J Linn Soc (Bot) 19:346, 1869.

Veligaster nitidum, as discussed by Guzmán and Tapia (1995), is a pantropical fungus. Characteristics that separate the genus Veligaster from Scleroderma following Guzmán (1969) are mainly the subgelatinous patches of the upper part of the stipe and base of the globose peridium. This fungus was confused with S. verrucosum Pers. (Guzmán 1970), a temperate species, that differs in lacking subgelatinous patches on the peridium and having larger spores, (10–)11–13(–14) µm diam. The spores of Veligaster nitidum are (7–)9–11(12) µm. The known distribution of V. nitidum was from Costa Rica, Cuba, Mexico and Nepal (type locality) (Guzmán and Tapia 1995). Scleroderma tenerum reported by Dennis (1970) from Venezuela seems to belong to Veligaster nitidum. This fungus is reported for the first time from the Virgin Islands on Guana Island. The material was collected on soil, in a forest under Pisonia subcordata Sw.

Specimens examined. – VIRGIN ISLANDS; Guana Island; Quail Dove Ghut, 16 Oct 1999, Lodge G-167 (GUA 266, XAL); N Beach Road., 15 Oct 1999, Lodge & Clum G-154 (GUA 252, XAL).

	ACKNOWLEDGMENTS

 
Guzmán thanks the Instituto de Ecología at Xalapa, CON-ACYT and SNI for the support of his research and Dr Laura Guzmán-Dávalos, Universidad de Guadalajara, Mexico, for her critical observations. He also thanks his assistants Fidel Tapia and Etelvina Gándara for their help in the microscopic study, Juan Lara Carmona for his herbarium assistance and María Eugenia Ramírez and Manuel Hernández for their computer help. Thanks also are given to the Kew Herbarium for the loan of important material. The research by Baroni, Miller and Lodge was supported by National Science Foundation grants (Biotic Surveys and Inventories Grants DEB-9525902 and DEB-01103621). Work in Puerto Rico was aided by NSF Grant BSR-8811902 of the Terrestrial Ecology Division of the University of Puerto Rico and the International Institute of Tropical Forestry at the Luquillo Experimental Forest Long Term Ecological Research Site.

	FOOTNOTES

 
Accepted for publication May 10, 2004.

¹ Corresponding author. E-mail: guzmang{at}ecologia.edu.mx

	LITERATURE CITED

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS LITERATURE CITED

 
Berkeley MJ. 1856. Decades of Fungi. Decades LXI–LXII. Rio Negro Fungi. Hooker’s J. Bot & Kew Garden Miscellany 8:272–280.

———, Cooke C. 1877. The fungi of Brazil, including those collected by J. W. H. Trail, Esq. M. A., 1874. J Linn Soc (Botany) 15:263–398.

Clements FE, Shear CL. 1957. The genera of Fungi. New York: Hafner. 496 p + 58 pls.

Coker WC. 1939. A new Scleroderma from Bermuda. Mycologia 31:624–626.

Dennis RWG. 1970. Fungus Floral of Venezuela and adjacent countries. Lehre: Cramer. 531 p.

Fischer E. 1933. Abteilung: Eumycetes (Fungi).-Klasse: Basidiomycetes. Unterklasse: Eubasidii, Reihe, Gasteromycetae In: Engler A, Prantl K, eds. Die Natürlichen Pflanzenfamilien, 7a, 2, Sweite & Auflage, Leipzig (reimpr. 1959, Duncker & Humblot, Berlin, p 1–22).

Garner JHB. 1956. Gasteromycetes from Panama and Costa Rica. Mycologia 48:757–764.

Guzmán G. 1967. Taxonomía del género Scleroderma Pers. emend. Fr. (Gasteromyc.). Ciencia 25:195–208.

———. 1969. Veligaster, a new genus of the Sclerodermataceae. Mycologia 61:117–123.

———. 1970. Monografia del género Scleroderma Pers. emend. Fr. (Fungi-Basidiomycetes). Darwiniana 16: 233–407.

———. 1983. Los hongos de la Península de Yucatán II. Nuevas exploraciones y adiciones micológicas. Biotica 8:71–100.

———. 1986. Distribución de los hongos en la región del Caribe y zonas vecinas. Caldasia 15:103–120.

———, Ovrebo CL. 2000. New observations on scleroder-mataceous fungi. Mycologia 92:174–179.

———, Tapia F. 1995. New species, new combinations and new records of Veligaster (Sclerodermataceae). Doc Mycol 25 (98–100):185–195.

Hennings P. 1904. Fungi Amazonici I. Ernest Ule collecti. Hedwigia 43:154–186.

Kornerup A, Wanscher JH. 1967. Methuen handbook of colour. London: Methuen and Co. 243 p.

Kreisel K. 1971. Clave para la identificacion de los macrom-icetos de Cuba. La Habana: Ser. A, Ciencias Biológicas 16, Universidad de La Habana. 101 p.

Lloyd CH. 1898–1926. Mycological Writings. 1–7, Cincinnati, Ohio.

Mattirolo O. 1921. Neo-saccardia nova Sclerodermataceae. Atti R Accad Sc Torino 56:7–33.

Patouillard N, Gaillard A. 1888. Champignons du Vénézué-la et principalement de la région du Haut-Orénoque, récolectés en 1887 por M. A. Gaillard. Bull Soc Mycol Fr 4:92–94 + 3 pls.

Petri L. 1900. Descrizione di alcuni gasteromicei di Borneo. Malpighia 14:111–139.

Reid DA. 1977. Some Gasteromycetes from Trinidad and Tobago. Kew Bull 31:657–690.

Standley PC. 1920–1926. Trees and shrubs of Mexico. Washington, D.C.: Contr U S Nat Herb 23, Smithsonian Institution (repr.1982, Vaduz: Cramer, 1721 p).

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This Article Abstract Full Text (PDF) Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Guzmán, G. Articles by Baroni, T. J. Search for Related Content PubMed Articles by Guzmán, G. Articles by Baroni, T. J. Agricola Articles by Guzmán, G. Articles by Baroni, T. J.