J. Hattori Bot. Lab. No. 76: 197-206 (Oct. 1994)

STUDIES IN THE FAMILY VI: THE AND PHYTOGEOGRAPHY OF DEL. S. LAT.

PERM. J0RGENSEN1

ABSTRACT. The Pannaria as presently understood is shown to be not homogeneous. It is divided in two genera: ( 1) Pannaria s. str., a tropical to warm-temperate, mostly foliose genus with no amyloid, apical structures in the asci, containing pannarin and related substances; it is further divided into three subgenera, of which subgenus Chryopannaria is newly described. (2) gen. nov., a temperate to arctic-alpine, mostly small-squamulose genus with amyloid apical structures in the asci, containing fatty acids and terpenoids; two subgenera are recognized, of which Micropannaria is newly described. All recognized species ( 16) in Fuscopa­ nnaria on the Northern Hemisphere are transferred to that genus.

INTRODUCTION In Zahlbruckner's ( 1927) lichen system, genera in the family Pannariaceae were distinguished artificially mainly on two sets of basic characters: ( 1) presence or absence of an apothecial thalline margin; (2) presence of green or blue-green algae. These two characters have for quite some time been known to be inadequate in establishing a satisfactory taxonomy for the genera. Henssen ( 1969) showed that the thalline margin of the Pannariaceae was of a very special nature, derived secondarily from the cortex of the thallus, and accordingly not at all of basic importance. Furthermore, James and Henssen (1975) gave many examples of species, durietzii P. James & Henssen being a notable case from the Pannariaceae, where a shift in photobiont occurred, which was simply environmentally induced and controlled. In my monograph of the European taxa (J0rgensen 1978) it was shown that the genus Pannaria was not homogeneous. However, no formal division was made at that time pending world wide studies undertaken to get a broader basis for a new taxonomy. In the 15 years which has passed, this has been achieved, and it is now possible to improve the taxonomy of the group, even though some problems still remain to be finally solved.

TAXONOMY J0rgensen (1978: 96- 99) divided European species of Pannaria into four informal groups: (1) the Psoroma hypnorum group, (2) the Pannaria rubiginosa group, (3) the Pannaria /eucosticta group, and ( 4) the Pannaria leucophaea group. Groups 2 (Panna­ ria s. str.) and 4 constitute the largest units, and are basically different (see Table 1), a fact confirmed by the non-European taxa. They differ in several basic, independent,

1 Botanical institute, Allegaten, 41 , N-5007 Bergen, Norway. 198 J. Hattori Bot. Lab. No. 76 I 9 9 4

Table 1. Pannaria s. str. and Fuscopannaria s. str. compared. Pannaria Fuscopannaria

Thall us Foliose to subfoliose, mostly bluish­ Squamulose to crustose, mostly grey brownish Chemistry Pannarin and/or related substance Fatty acids and terpenes (rarely (rarely none) none) Apothecia With distinct thalline margin With varying thalline margin Hymenium I - , except in the vicinity of asci I + blue-green, turning red-brown Asci Without amyloid apical structures With amyloid apical plug Distribution Pantropical to warm temperate Temperate mainly Northern Hemisphere correlated characters, most importantly in ascus structure (Figs. 1, 2), and chemistry both of the hymenia and the thallus. They clearly constitute two different genera and accordingly group 4 is newly described as Fuscopannaria P. M. J0rg. below. The name is derivated from fuscus = brown, because many of the species normally have a brownish thallus. The species are often more small-squamulose than those of Pannaria s. str., and interestingly, Fuscopannaria is the genus with the most variable thalline margin of the apothecia, sometimes completely lacking, sometimes present even on specimens of the same species. Species of Pan.naria s. str. all invariably have a well developed thalline margin, while it is absent in all species of Parmelie/la, with only one notable exception: mariana (Fr.) P. M. J0rg. & D. J. Galloway. Fuscopannaria is more closely related to Psoroma s. str. (Type: Psoroma hypnorum (Yahl) S. F. Gray) than toPannaria. Species of Psoroma s. str. which are also brownish and small-squamulose, have the same main type of apical apparatus in the asci, though the manubrium is broader, with a different hymenial and thalline chemistry (see J0rgensen 1978: 27- 28). (Larger leafy, more tropical species presently included in Psoroma, such as Psoroma sphinctrinum (Mont.) Nyl., does not belong in that genus. Their taxonomic position will be discussed in a separate paper). While this division of the genus Pannaria s. lat. into two is clearcut and un­ problematical, some further problems remain relating to the position of Pannaria pezizoides (G. H. Weber) Trevis. (in group 1), P. hookeri (Sm.) Nyl. (in group 2) and the species of group 4 (P. leucophaea (Yahl) P. M. J0rg. and P. saubinetii (Mont.) Nyl.) in this new system. These are all small-squamulose species with little or no thalline chemistry in their thalli, and they occur outside the main distribution area of Pannaria s. str. The most deviating species in this respect are P. hookeri and its Southern Hemisphere relative P. dichroa (J. D. Hook.) Nyl., growing in the polar regions (see Fig. 9). They are also unusual in other respects, mostly resembling species of Lecanora because of their nearly crustose thalli and dark, often black, apothecia. Anatomically they are distinctive in having a thick cortex of thick-walled cells (see J0rgensen 1978: 22), incorporating dead cells from the very dense and massive cyanobiont layer, and a dense medulla of horizontally aligned hyphae. Henssen ( 1969: 24 7) also found a difference from Pannaria s. str. in the later stages of the apothecial ontogeny. However, P. M. J O RGENSEN: Studies in the li chen famil y Pannoriaceae VI 199 the ascus-type is the same as in Pannaria s. str., with no amyloid apical structures, and the hymenial reactions are also identical: I + persistantly deep blue, mainly in the vicinity of the asci. The thallus contains pannarin, though sometimes in small quantities (rarely completely lacking). Thus, there is no doubt that P. hookeri and P. dichroa are closely related to Pannaria, in spite of their aberrant morphology and phytogeography. I therefore prefer to keep them within the genus, but placed in a separate subgenus. Pannaria pezizoides presents a more difficult problem. J 0rgensen ( 1978: 97) grouped it, with some hesitation, together with Psoroma hypnorum. These two species have so many characters in common that James and Henssen ( 1976: 4 7- 48) suspected that they might constitute a phototype pair. They both have small-squamulose thalli with no chemistry, overgrowing bryophytes, often occurring side by side. Their apothecia are large with I + blackish-blue reaction of the hymenia and they have uniquely warted, large spores. However, Pannaria pezizoides lacks the distinct amyloid apical structures of Psoroma hypnorum, and accordingly has an ascus rather similar to that of Pannaria s. str. We have here either a case of extreme convergence of the genera Pannaria and Psoroma, or a loss of the amyloid reaction of the apical structures in the asci in one species of Psoroma. Although I suspect the latter to be the case, I do not want to transfer P. pezizoides to Psoroma before conclusive evidence is available. Therefore for the time being I follow Gyelnik ( 1940) in placing P. pezizoides in a subgenus of its own within Pannaria, where it has an isolated position. Hopefully studies of the microstructures of the asci may reveal characters of importance for the final solution of this taxonomic dilemma. Species of group 4, P. /eucophaea and P. saubinetii , are as previously pointed out (forgensen 1978: 99) closely related to those of group 3, i.e. Fuscopannaria. Both morphologically and anatomically they are quite similar. Even the reaction of the hymenium, I + blue-green rapidly changing to red-brown, is the same. The amyloid apical apparatus of the asci is, however, sheet-like (see Fig. 3) and not a plug as in the species of Fuscoderma. This is the only clear difference from that genus; the two species are even found within the main distribution area of Fuscoderma (see below). In an ascus without apical thickening, plug-like structures would have no room, and therefore a sheet-like structure may be interpreted as a modification of a plug due to these circumstances. In my opinion one must allow even apical structures to vary somewhat within one genus, just as other characters do. In this case there is no indication of any other correlating differences, and I therefore include group 4 in Fuscopannaria on subgeneric level.

TAXONOMIC CONCLUSIONS In accordance with the data and interpretations presented above, the following taxonomy of Pannaria s.lat. is presently proposed: I. Pannaria Delise in Bory, Diet. Class. Hist. Nat. 13: 20 (1828). Type species: Pannaria rubiginosa (Ach.) Bory (see Fig. 4), lectotype by Dodge 1933: 441 (the one by Fink ( 1910: 150) is mechanical, being selected by the first species rule, and Clements' and Shear's ( 1931 : 323) choice of P. pezizoides incorrect, as this was not 200 J. Hattori Bot. Lab. o. 76 I 9 9 4

Figs. 1- 4. I. Ascus of Pannaria rubiginosa with no internal amyloid, apical structures. Photo: G . Rambold. 2. Ascus of Fuscopannaria leucosticta with an internal, amyloid plug apically. Photo: G. Rambold. 3. Ascus of Fuscopa1111aria leucophaea with an internal, amyloid sheet. Photo: G . Rambold. 4. Pannaria rubiginosa , type specis of the genus Pannaria. Photo: Jan Berge. P. M. 10RGENSEN: Studies in the lichen fami ly Pannoriaceae VI 201

Fig. 5- 8. 5. Pannaria hookeri, type species of the subgenus Chryopannaria . Photo: Jan Berge. 6. Pannaria pezizoides, type species of the subgenus . Photo: Jan Berge. 7. Fuscopannaria leucosticta, type species of the genus Fu scopannaria . Photo: Jan Berge. 8. Fuscopannaria leucophaea , type species of subgenus Micropannaria . Photo: Jan Berge. 202 J. Hattori Bot. Lab. No. 76 I 9 9 4

one of the original species). 1. Subgenus Pannaria, type as above. 2. Subgenus Chryopannaria P. M. J0rg., subgen. nov. Thallus crustaceus, cortex cellulis crassoparietaris; stratum cyanobacterium densum. Apothecia atra. In regionibus arcticis et antarcticis crescens. Typus subgenericus: Pannaria hookeri (Borrer ex. Sm.) Ny!. (see Fig. 5). 3. Subgenus Protopannaria Gyelnik in Rabenhorst: Krypt. Flora 9, Abt.2, Tei! 2: 216 ( 1940). Type species: Pannaria pezizoides (G. H. Weber) Trevis. (see Fig. 6), holotype. II. Fuscopannaria P. M. Jorg., gen. nov. Thallus squamulosus, plusminusque fuscus, acida pinguia et terpeni (seu nullus) continens. Hymenium in iodo cyaneum deinde rubescens coloratum. Asci tholis amyloideis. Typus genericus: Fuscopannaria leucosticta (Tuck. in Dari.) P. M. J0rg. (see below p. and Fig. 7). l. Subgenus Fuscopannaria, type as above. 2. Subgenus Micropannaria P. M. Jorg., subgen. nov. Subgeneris Fuscopannariae similis, sed asci Stratis amyloideis apicalis. Typus subgenericus: Fuscopannaria leucophaea (Yahl) P. M. J0rg. (see below p. OOO and Fig. 8).

PHYTOGEOGRAPHY Pannaria s.str., as presently understood, is a small genus of a dozen species, most of which are pantropical with a few temperate species (see Fig. 9). The distribution pattern is rather similar to that shown by Coccocarpia (Arvidsson 1983: 35), the most obvious difference being the extention northwards in western Europe, to Finnmark in Norway, caused by the two temperate species P. rubiginosa and P. conoplea (Ach.) Bory. The genus is particularly well represented and diverse in the paleotropics with a major area of diversity in Australasia with ten species, four of which are endemic to Australia. In Africa the genus is also well-represented with seven species, two of which are endemic, including the very interesting narrow endemic P. santessonii Krog & Swinscow from East Africa, which has a thallus organized rather like a Leptogium with a one-cell layered cortex and a swelling cyanobiont layer (Swinscow & Krog 1986). This latter feature is characteristic of several of the most tropical species, those of the P. lurida (Mont.) Ny!. group. South America has a smaller number of species (5) with only one endemic, P. mosenii Dodge (incorrectly also mentioned from E. Africa by Jorgensen 1978: 115). This has interestingly developed another growth-form typical of several tropical lichen species, e.g. Parmeliella mariana: a rosette of a narrow-lobed thallus resting on a mat of moisture-retaining rhizohyphae. In the Northern Hemisphere, mainland Asia, North America and Europe only 3- 4 species are present, and none of them endemic, clearly confirming the tropical origin of the genus Pannaria. Most anomalous in this connection is the Arctic/Antarctic, strongly bipolar subg. P. M. 10RGENSEN: Studies in the lichen family Pannoriaceae VI 203

Pannaria subg. Pannaria e Pannaria subg. Arctopannaria 0 Fig. 9. Distribution map of the genus Pannaria subg. Pannaria (hatched area and black dots) and subg. Chryopannaria (dark area and open dots).

Chryopannaria with two species in the Southern Hemisphere, P. dichroa and P. hookeri and one in the Northern: P. hookeri. The tricentric distribution pattern in the Southern Hemisphere, with a presence also on that very old island Kerguelen, is usually interpretated as a sign of great age (forgensen 1983: 63) and it is likely that the subgenus originated in the Southern Hemisphere. Possibly it branched off fairly early in the development of the genus, and adapted (or was well adapted) to the harsh conditions in the (sub) antarctic region. Its presence in the Northern Hemisphere is difficult to explain without postulating long distance dispersal, as there are no records from the mountain chains in America or Asia indicating "mountain-jumping". P. hookeri reaches only as far south as the Alps, and occurs there only on the highest peaks. The nearest occurrence in the Southern Hemisphere is on the subantarctic Prince Edward Islands (SE of S. Africa)! The distribution of subg. Protopannaria has not been mapped since the taxonomic position of P. pezizoides is so uncertain. It is widely distributed in temperate to arctic regions of the Northern Hemisphere with only two reliable records from the Southern Hemisphere, one from Uganda at 4400m alt. at the Equator (forgensen 1978: 53) and one old collection from St. Helena (Galloway 1994). Fuscopannaria with about twenty species is, unlike Pannaria s. str., mainly a temperate genus, mostly found in the Northern Hemisphere (Fig. 10) with two principal areas of speciation: Pacific North America and Atlantic-Mediterranean 204 J. Hattori Bot. Lab. No. 76 I 9 9 4

Fig. 10 Distribution map of the genus Fuscopannaria.

Europe. This pattern is usually interpreted as a Tertiary relict one, the type species of the genus F. leucosticta being a particularly good example of this (see forgensen 1978: 107). There are nine species in Pacific North America (and still some to be clarified), three of which are endemic to the region. Atlantic-Mediterranean Europe has nine species (also found in adjacent North Africa), four of which are endemic. Two of these, F. ahlneri (P. M. forg.) P. M. forg. and F. confusa (P. M. forg.) P. M. forg. are confined to moist boreal forests. The latter, recently described (J0rgensen 1991), is as yet only known from Europe, while F. ahlneri has also been found on the east coast of North America as well as on the northern Pacific coasts of East Asia and North America. One species F. praetermissa (Nyl.) P. M. forg., is arctic-alpine and is widespread on the Northern Hemisphere, and also present in the Himalayas. The genus is also present in the Southern Hemisphere with three closely related, endemic species in Australasia, linked with the main distribution area across the SE Asian islands (Phillippines and New Guinea). In southern South America two further species are known. Their status and relationship to the taxa in Australasia is currently under investigation, but they are most probably closely related to these and appear to have arrived in South America via western Antarctica (see e.g. J0rgensen 1983). The species of subg. Micropannaria follow the above-mentioned pattern: F. saubi­ netii (Mont.) P. M. J0rg. is disjunctive between Mediterranean European and Pacific North America, while F. leucophaea is widespread in the Northern Hemisphere (see J0rgensen 1978:41). From this I conclude that the genera Pannaria and Fuscopannaria with their P. M. JORGENSEN: Studies in the lichen family Pannoriaceae VI 205 dissimilar distribution patterns have different evolutionary centers.

TAXONOMIC TREATMENTS As a consequence of the taxonomic views presented above, the following new combinations for species in the Northern Hemisphere are necessary. Most of these taxa are treated in my monograph (forgensen 1978). In addition to those included in the following list, there are some critical and poorly understood taxa of Fuscopannaria in the Pacific region of East Asia and North America which I hope to be able revise in the near future. Taxa from the Southern Hemisphere will be treated separately. Fuscopannaria ahlneri (P. M. forg.) P. M. forg., comb. nov. Pannaria ahlneri P. M. forg., Opera Bot. 45: 15 (1978). Fuscopannaria confusa (P. M. J0rg.) P. M. J0rg., comb. nov. Pannaria confusa P. M. forg., Ann. Bot. Fenn. 28: 87 (1991). Fuscopannaria ignobilis (Anzi) P. M. J0rg., comb. nov. Pannaria ignobilis Anzi, Comment. Soc. Critt. ltal. 1: 138-139 (1862). Fuscopannaria Jaceratula (Hue) P. M. J0rg., comb. nov. Pannaria Jaceratula Hue, Bull. Bot. Soc. France 46: 59 (1902). Fuscopannaria leucophaea (Yahl) P. M. forg., comb. nov. Lichen Jeucophaeus Yahl, Flora danica 6, fasc.16: 8 ( 1787). Fuscopannaria leucosticta (Tuck.) P. M. J0rg., comb. nov. Pannaria Jeucosticta Tuck. in Darlington: Flora cestrica 3. ed.: 441 (1853). Fuscopannaria leucostictoides (K. Ohlsson) P. M. J0rg., comb. nov. Pannaria /eucostic­ toides K. Ohlsson, The Bryologist 76: 379- 380 (1973). Fuscopannaria maritima (P. M. J0rg.) P. M. J0rg., comb. nov. Pannaria maritima P. M. forg., Opera Bot. 45: 114 (1978). Fuscopannaria mediterranea (C. Tav.) P. M. J0rg., comb. nov. Pannaria mediterranea C. Tav., Port. Acta Biol. (B) 8: 5- 6 (1965). Fuscopannaria o/ivacea (P. M. J0rg.) P. M. J0rg., comb. nov. Pannaria o/ivacea P. M. forg., Opera Bot. 45: 49 (1978). Fuscopannaria poeltii (P. M. J0rg.) P. M. forg., comb. nov. Pannaria poeltii P. M. forg., Opera Bot. 45: 115 (1978). Fuscopannaria praetermissa (Nyl.) P. M. J 0rg., comb. nov. Pannaria praetermissa Nyl. in Chydenius & Furuhjelm, Not. Sallsk. Flora & Fauna Fenn. 4: 97 (1858). Fuscopannaria protensa (Hue) P. M. J0rg., comb. nov. Pannaria protensa Hue, Nouv. Arch. Mus., ser. 4, 10: 182 (1909). Fuscopannaria pulveracea (P. M. J0rg. & Henssen) P. M. J0rg., comb. nov. Pannaria pulveracea P. M. forg. & Henssen, Opera Bot. 45: 115 (1978). Fuscopannaria sampaiana (C. Tav.) P. M. J0rg., comb. nov. Pannaria sampaiana C. Tav., Port. Acta Biol. (B) 3: 76-77 (1950). Fuscopannaria saubinetii (Mont.) P. M. J0rg., comb. nov. saubinetii Mont., Ann. Sci. Nat. Bot. ser. 2, 6: 331 (1836). 206 J. Hattori Bot. Lab. No. 76 I 9 9 4

ACKNOWLEDGEMENTS I am indebted to the organizers of the symposium for inviting me to present this paper. A grant from NAVF (The Norwegian Research Council) made it possible to finalize these studies during a sabbatical in London, and one from the University of Bergen enabled me to attend the meetings. I am most thankful for this support. I am further indebted Dr. Gerhard Rambold, Miinchen for providing me with photographs of the apical structures and for discussions on their interpretation. Finally my sincerest thanks to Mr. J. Berge, Bergen who kindly photographed the specimens, and Dr. D. J. Galloway who made comments on the manuscript.

R EFERENCES Arvidsson, L. 1983. A monograph of the lichen genus Coccocarpia. Opera Bot. 67 . Clements, F. E. & C. L. Clements. 1931. The genera of fungi . New York. Dodge, C. W. 1933. The foliose and fruticose of Costa Rica I. Ann. Miss. Bot. Garden 20: 373- 467. Fink, B. 1910. The lichens of Minnesota. Contr. U. S. Natl. Herb. 14, l. Galloway, D. 1994. Lichen collections of Archibald Menzies MD, FLS (1754- 1842). Edin. Journ. Bot. (in press). Henssen A. 1969. Die Entstehung des Thallusrandes bei den Pannariaceen (Lichenes). Ber. Deutsche Bot. Ges. 82: 235-248. James, P. W. & A. Henssen. 1975. The morphological and taxonomical significance of cephalo­ dia. In D. H. Brown, D. L. Hawksworth & R. H. Bailey (eds.), Lichenology: Progress and Problems: 27- 77. J0rgensen, P. M. 1978. The lichen family Pannariaceae in Europe. Opera Bot. 45. fargensen, P. M. 1983. Distribution patterns of lichens in the Pacific region. Austr. Journ. Bot. Suppl. ser 10: 43- 66. J0rgensen, P. M. 1991. Studies in the lichen family Pannariaceae V. On some Fennoscandian Pannaria species. Ann. Bot. Fenn. 28 : 87-91. Swinscow, T. D. V. & H. Krog. 1986. Some observations on the thallus in Pannaria , with description of a new species. Lichenologist 18 : 309- 317. Zahlbruckner, A. 1926. Lichenes (Flechten). B. Spezieller Teil. In A. Engler & K. Prantl (eds.), Die natiirlichen Pflanzenfamilien 8: 61 - 270.