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Battarrina inclusa - a rarely found fungus within a fungus
N%& &KJ
Battarrina inclusa - a rarely found fungus within a fungus "$%!#&H%"$ B hilst on the Justin Smith memorial foray based in Minehead Sept 2015 I collected a group of Tuber puberulum fruitbodies close to Fagus sylvatica and Castanea sativa. In the lab these were checked out; first by ensuring the spores were globose and reticulate and then by checking the peridium, which has a pseudoparenchymatous structure of subglobose elements. Sections were taken and spores were confirmed as appropriate. The peridium section was odd, it looked as if I hadn’t cleaned the slide and cover slip properly. What I could see under low power was masses of what appeared to be conidia, though some were stacked in what appeared to be asci and others floating free. A clean slide and coverslip were obtained and a new section made. It was the same; what was it? I recalled a discussion I had had with Paul Cannon some eighteen months earlier. He had asked if I ever got parasitic fungi in my hypogeous collections. I had replied no and what did they look like? Was this what I had found? With no internet access in the lab I returned to the hotel to research my find. This turned out to be surprisingly easy for such an obscure collection, the wonders of the web provided an answer within minutes. Battarrina inclusa was illustrated (Fig. 1.) and briefly described by Berkeley and Broome (1861) in Annals and Magazine of Natural History as Hypocrea inclusa Berk. & Broome. The holotype was collected by C. E. Broome in September 1859 in Leigh Woods near Bristol within Tuber puberulum K(M)200651. Saccardo (1883) subsequently placed Hypocrea inclusa in a new subgenus because of the rounded spores and named the subgenus Battarrina after Giovanni Antonio Battarra. It became known, incorrectly, as Battarrina inclusa (Berk. & Broome )Sacc.; incorrect because he had not moved it to a new genus. Recognising this, Clements in Clements and Shear (1931) raised Battarrina to generic
level and it became Battarrina inclusa (Berk. & Broome ) Clem.
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As only two collections from the UK were shown in RBG Kew Herbtrack, both made by Broome, I had originally thought that my collection was the third. His holotype had not at that time been digitised, but has now also been entered on Herbtrack. However research for this paper unearthed further information. I discovered that Hawker (1955) had also collected specimens in 1953 (in her collection as Hawker 968). She comments on the poor spore illustration in ‘Annals’, which I had intended to draw to the reader’s attention and describes the spores as being “minutely and sparsely echinulate”. She also comments on the spores illustrated in Petch (1938) being also incorrect as they are drawn with a halo around them.
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doi: 10.1016/j.fldmyc.2016.01.007
2,
N%& &KJ A further paper by Thoen & Schultheis (2005) describes the species in great detail and has electron micrographs of the spores and other good illustrations. These show that the spores have a minute raised reticulation which is almost impossible to see even with a good light microscope. With a light microscope at x 1000 the spores appear as Hawker (1955) described, though under DIC microscopy (Differential Interference Contrast) I have managed to discern the reticulation. No doubt a Victorian microscopist would have been further handicapped and would have been unable to resolve this reticulation. Thoen & Schultheis (2005) studied two collections of their own from Luxembourg and two further collections from herbaria. Material of Tuber puberulum from Broome’s third collection of 1871 had been circulated by Rabenhorst to l’herbier du Jardin Botanique National de Belgique and to the Swedish Museum of Natural History but neither was found to contain Battarrina inclusa. They did not study the holotype, as an earlier paper by Rossman et al. (1999) described the Kew material as having been preserved in liquid and then dried, and thus in poor condition. Two further recent collections from Europe are also illustrated on the internet: firstly a collection from Spain made by C. Gelpi and illustrated by Enrique Rubio on Ascofrance (www. ascofrance.fr), supposedly collected from within Tuber cistophilum on 5/05/2013, secondly Paco Sáinz and Pedro M. Pasaban’s excellent internet
site Hongos Hippogeos (https://sites.google. com/site/hongoshipogeos/) showing material collected in Tuber puberulum. Although my research has unearthed a number of references, it is unlikely that there are many other European collections of this species. Details of my collection Battarrina inclusa (Berk. & Broome) Clem. K(M)202531 Approximately twenty mature and immature fruitbodies of Tuber puberulum were collected in a cluster on 24/09/2015 at Broad Oak Hill, ST134345 South Somerset, at the edge of a road, associated with Castanea sativa and Fagus sylvatica. Most fruitbodies appear to be infected with the parasite Battarrina inclusa (Fig. 2) but they also have normal T. puberulum asci and spores within them. Although initially, under poor light, the specimens did not appear to be abnormal morphologically, in section they contained the parasite. When dried they shrank substantially more than normal and appear when dried slightly lumpy and translucently mottled (Fig. 3.)
Microscopy in ammonia or water (for measurements). Perithecia appear as slightly honey coloured domes up to approx 250–300 µm diameter (measured across preparation) embedded in the gleba of T. puberulum. Asci approximately 40 x 5 µm containing 8 spores, mostly uniseriate. Paraphyses in some cases double the length of the asci, filiform, approx 0.8 µm wide, up to 72 µm long. Spores are easily seen as the ascus appears to break up rather than discharge, although I did find one empty ascus. Spores are enclosed within the perithecia. Spores globose with reticulation 3–4 µm (Fig. 4.). Presumably dispersal is by disintegration of the fruitbody, or by animal ingestion. I found one collection which was both disintegrating and being eaten by maggots. Substantial numbers of spores were released within the preparation. Thoen & Schultheis (2005) & & #$ #PO& %M!& " & "$" #& "!& %$#& P!& : raised a number of points in their O$%% & % %$" && &H%"$
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N%& &KJ paper. Their material was collected at different times of year from the British collections, in December and March. My collection and Broome’s 1859 collection were collected in September and other British material was collected in November. I don’t think this is particularly significant as I have found hypogeous material at various times of the year and variability is I believe dependent on weather patterns. They also pointed out that Rossman et al. (1999) had no molecular evidence for placing Battarrina into Bionectriaceae. Lastly they asked the question, how did the parasite get into the host fruitbody? It was clear from my material that some of the younger specimens were not maggot ridden and did not appear to have been damaged so entry must have been during early development, maybe through the mycelium or at the primordia stage.
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References
Acknowledgments This paper is dedicated to the memory of Justin Smith 1967–2014. With thanks to Alick Henrici for his continued help, supplying additional information from RBG Kew.
Berkeley, M.J. & Broome, C.E. (1861). Notices of British Fungi. Annals and Magazine of Natural History, Ser. 3, 7: 449– 456. [Image downloaded from: The Biodiversity Heritage Library. Digitized by [Gerstein - University of Toronto (archive.org)]. www.biodiversitylibrary.org.]
Clements, F.E. & Shear, C.L., (1931). The Genera of Fungi. New York. H.W. Wilson. Hawker, L. E. (1955). Hypogeous fungi IV & V. Trans. Brit. Mycol. Soc. 38: (I)73–77. Petch, T. (1938). British Hypocreales. Trans. Br. Mycol. Soc. 21: 243–305. Rossman, A.Y., Samuels, G.J., Rogerson, C.T. & Lowen, R. (1999). Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud. Mycol. 42: 1–248. Saccardo, P.A. (1883). Sylloge Fungorum omnium hucusque cognitorum, Vol. II. Padua. 815, LXX, 77p. [Image from the Biodiversity Heritage Library. Digitized by [New York Botanical Garden LuEster T.Merz library]. www.biodiversitylibrary.org.]
Thoen, D. & Schultheis, B. (2005). Battarrina inclusa, une très rare Hypocréale commensale ou parasite de Tuber puberulum, découverte au Grand-Duché de Luxembourg. Syst. Geogr. Pl. 75: 25–34.
Internet references https://sites.google.com/site/hongoshipogeos/asc omycetes/battarrina-inclusa-berk-broomeclem-1931 http://www.ascofrance.com/search_recolte/3485
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Battarrina inclusa - a rarely found fungus within a fungus "$%!#&H%"$ B hilst on the Justin Smith memorial foray based in Minehead Sept 2015 I collected a group of Tuber puberulum fruitbodies close to Fagus sylvatica and Castanea sativa. In the lab these were checked out; first by ensuring the spores were globose and reticulate and then by checking the peridium, which has a pseudoparenchymatous structure of subglobose elements. Sections were taken and spores were confirmed as appropriate. The peridium section was odd, it looked as if I hadn’t cleaned the slide and cover slip properly. What I could see under low power was masses of what appeared to be conidia, though some were stacked in what appeared to be asci and others floating free. A clean slide and coverslip were obtained and a new section made. It was the same; what was it? I recalled a discussion I had had with Paul Cannon some eighteen months earlier. He had asked if I ever got parasitic fungi in my hypogeous collections. I had replied no and what did they look like? Was this what I had found? With no internet access in the lab I returned to the hotel to research my find. This turned out to be surprisingly easy for such an obscure collection, the wonders of the web provided an answer within minutes. Battarrina inclusa was illustrated (Fig. 1.) and briefly described by Berkeley and Broome (1861) in Annals and Magazine of Natural History as Hypocrea inclusa Berk. & Broome. The holotype was collected by C. E. Broome in September 1859 in Leigh Woods near Bristol within Tuber puberulum K(M)200651. Saccardo (1883) subsequently placed Hypocrea inclusa in a new subgenus because of the rounded spores and named the subgenus Battarrina after Giovanni Antonio Battarra. It became known, incorrectly, as Battarrina inclusa (Berk. & Broome )Sacc.; incorrect because he had not moved it to a new genus. Recognising this, Clements in Clements and Shear (1931) raised Battarrina to generic
level and it became Battarrina inclusa (Berk. & Broome ) Clem.
W
& &P $" %!& & 9 &E$%%O#&%&#$ #PO&"! %$#& %&
+ & $#$%P#& $%O E#$I## &"!&E$%%O#&K=>J
As only two collections from the UK were shown in RBG Kew Herbtrack, both made by Broome, I had originally thought that my collection was the third. His holotype had not at that time been digitised, but has now also been entered on Herbtrack. However research for this paper unearthed further information. I discovered that Hawker (1955) had also collected specimens in 1953 (in her collection as Hawker 968). She comments on the poor spore illustration in ‘Annals’, which I had intended to draw to the reader’s attention and describes the spores as being “minutely and sparsely echinulate”. She also comments on the spores illustrated in Petch (1938) being also incorrect as they are drawn with a halo around them.
B=A&L "%$&D%" &L ## &L%P &3%$I $#&L&L
doi: 10.1016/j.fldmyc.2016.01.007
2,
N%& &KJ A further paper by Thoen & Schultheis (2005) describes the species in great detail and has electron micrographs of the spores and other good illustrations. These show that the spores have a minute raised reticulation which is almost impossible to see even with a good light microscope. With a light microscope at x 1000 the spores appear as Hawker (1955) described, though under DIC microscopy (Differential Interference Contrast) I have managed to discern the reticulation. No doubt a Victorian microscopist would have been further handicapped and would have been unable to resolve this reticulation. Thoen & Schultheis (2005) studied two collections of their own from Luxembourg and two further collections from herbaria. Material of Tuber puberulum from Broome’s third collection of 1871 had been circulated by Rabenhorst to l’herbier du Jardin Botanique National de Belgique and to the Swedish Museum of Natural History but neither was found to contain Battarrina inclusa. They did not study the holotype, as an earlier paper by Rossman et al. (1999) described the Kew material as having been preserved in liquid and then dried, and thus in poor condition. Two further recent collections from Europe are also illustrated on the internet: firstly a collection from Spain made by C. Gelpi and illustrated by Enrique Rubio on Ascofrance (www. ascofrance.fr), supposedly collected from within Tuber cistophilum on 5/05/2013, secondly Paco Sáinz and Pedro M. Pasaban’s excellent internet
site Hongos Hippogeos (https://sites.google. com/site/hongoshipogeos/) showing material collected in Tuber puberulum. Although my research has unearthed a number of references, it is unlikely that there are many other European collections of this species. Details of my collection Battarrina inclusa (Berk. & Broome) Clem. K(M)202531 Approximately twenty mature and immature fruitbodies of Tuber puberulum were collected in a cluster on 24/09/2015 at Broad Oak Hill, ST134345 South Somerset, at the edge of a road, associated with Castanea sativa and Fagus sylvatica. Most fruitbodies appear to be infected with the parasite Battarrina inclusa (Fig. 2) but they also have normal T. puberulum asci and spores within them. Although initially, under poor light, the specimens did not appear to be abnormal morphologically, in section they contained the parasite. When dried they shrank substantially more than normal and appear when dried slightly lumpy and translucently mottled (Fig. 3.)
Microscopy in ammonia or water (for measurements). Perithecia appear as slightly honey coloured domes up to approx 250–300 µm diameter (measured across preparation) embedded in the gleba of T. puberulum. Asci approximately 40 x 5 µm containing 8 spores, mostly uniseriate. Paraphyses in some cases double the length of the asci, filiform, approx 0.8 µm wide, up to 72 µm long. Spores are easily seen as the ascus appears to break up rather than discharge, although I did find one empty ascus. Spores are enclosed within the perithecia. Spores globose with reticulation 3–4 µm (Fig. 4.). Presumably dispersal is by disintegration of the fruitbody, or by animal ingestion. I found one collection which was both disintegrating and being eaten by maggots. Substantial numbers of spores were released within the preparation. Thoen & Schultheis (2005) & & #$ #PO& %M!& " & "$" #& "!& %$#& P!& : raised a number of points in their O$%% & % %$" && &H%"$
2%
N%& &KJ paper. Their material was collected at different times of year from the British collections, in December and March. My collection and Broome’s 1859 collection were collected in September and other British material was collected in November. I don’t think this is particularly significant as I have found hypogeous material at various times of the year and variability is I believe dependent on weather patterns. They also pointed out that Rossman et al. (1999) had no molecular evidence for placing Battarrina into Bionectriaceae. Lastly they asked the question, how did the parasite get into the host fruitbody? It was clear from my material that some of the younger specimens were not maggot ridden and did not appear to have been damaged so entry must have been during early development, maybe through the mycelium or at the primordia stage.
&A &L%$#&%&& + M #$#&%!#&"!&2P &#$! #&P$"#&$# P" %! & % %$" && &H%"$
References
Acknowledgments This paper is dedicated to the memory of Justin Smith 1967–2014. With thanks to Alick Henrici for his continued help, supplying additional information from RBG Kew.
Berkeley, M.J. & Broome, C.E. (1861). Notices of British Fungi. Annals and Magazine of Natural History, Ser. 3, 7: 449– 456. [Image downloaded from: The Biodiversity Heritage Library. Digitized by [Gerstein - University of Toronto (archive.org)]. www.biodiversitylibrary.org.]
Clements, F.E. & Shear, C.L., (1931). The Genera of Fungi. New York. H.W. Wilson. Hawker, L. E. (1955). Hypogeous fungi IV & V. Trans. Brit. Mycol. Soc. 38: (I)73–77. Petch, T. (1938). British Hypocreales. Trans. Br. Mycol. Soc. 21: 243–305. Rossman, A.Y., Samuels, G.J., Rogerson, C.T. & Lowen, R. (1999). Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud. Mycol. 42: 1–248. Saccardo, P.A. (1883). Sylloge Fungorum omnium hucusque cognitorum, Vol. II. Padua. 815, LXX, 77p. [Image from the Biodiversity Heritage Library. Digitized by [New York Botanical Garden LuEster T.Merz library]. www.biodiversitylibrary.org.]
Thoen, D. & Schultheis, B. (2005). Battarrina inclusa, une très rare Hypocréale commensale ou parasite de Tuber puberulum, découverte au Grand-Duché de Luxembourg. Syst. Geogr. Pl. 75: 25–34.
Internet references https://sites.google.com/site/hongoshipogeos/asc omycetes/battarrina-inclusa-berk-broomeclem-1931 http://www.ascofrance.com/search_recolte/3485
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