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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by RERO DOC Digital Library The Lichenologist 45(1): 77–87 (2013) 6 British Lichen Society, 2013 doi:10.1017/S0024282912000631 New morphological aspects of cephalodium formation in the lichen Lobaria pulmonaria (Lecanorales, Ascomycota) Carolina CORNEJO and Christoph SCHEIDEGGER Abstract: Cephalodia were investigated on young and mature thalli of Lobaria pulmonaria. Cephalodia originate from contact between hyphae and cyanobacteria on the upper or lower cortex or, less frequently, in the apical zone. Young thalli were found to associate with cyanobacteria even in the anchoring zone. Cephalodia formed on the young thalli or the anchoring hyphae share the same phenotypic characteristics. In spite of being composed of paraplectenchymatous hyphae, the cortex of mature thalli preserves a considerable plasticity, enabling the formation of cephalodia. The cyano- bacterial incorporation process begins with cortical hyphae growing out towards adjacent cyanobac- terial colonies, enveloping them and incorporating them into the thallus. The incorporation process is the same on the upper and the lower cortex. Early stages of cephalodia are usually found in young lobes, whereas in the older parts of the thallus only mature cephalodia are found. Key words: cephalodia, cephalodiate lichen, Nostoc, tripartite lichen Accepted for publication 26 June 2012 Introduction Cephalodia were first classified by Nylander (1868) as epigenic, hypogenic or endogenic. There has been heated debate over the na- This categorization assumes that cephalodia ture of cephalodia for more than 50 years. are found where they originated. Winter Forsell (1884) was the first to propose that (1877) and Forsell (1884), however, noticed cyanobacteria are incorporated actively by that cephalodia, which form on the lower the mycobiont and do not penetrate into the cortex, could grow into the thallus. This thallus by themselves. Thus, in contrast to means that the thalloid position of cepha- other contemporary authors, he considered lodia does not necessarily correspond to cephalodia to be part of the symbiotic pheno- their point of origin. Later authors followed type and not parasitic (Winter 1877; Moreau Nylander’s classification, with diverse modi- 1921; Kaule 1932). Forsell (1884) defined fications related to the species studied and cephalodia as formations of the lichen thallus without the misleading term endogenic. which contain algae of a different kind to Jordan (1970) called a superior cephalodium those found in the algal layer, and which a protuberance located on the upper surface, evolve by the interaction of hyphae with these and the author used inferior for a cephalo- algae. Today it is generally accepted that a dium situated on the lower cortex. Recent cephalodium is a specialized protuberance, a works refer to cephalodia simply as internal, gall-like structure of the vegetative thallus if located in the medulla, or external, if found that includes a cyanobacterium in a symbio- on the upper or lower cortex (Henssen & tic relationship ( Jordan 1970; Jahns 1988; Jahns 1974; Rikkinen et al. 2002). Paulsrud et al. 1998; Honegger 2001). During the 19th and early 20th centuries, a considerable amount of research was carried out on developmental questions of cephalo- dia. Although Winter (1877) was an advo- C. Cornejo and C. Scheidegger: Swiss Federal Institute cate of the parasite-hypothesis of cephalodia, for Forest, Snow and Landscape Research WSL, 8903 Birmensdorf, Switzerland. Email: [email protected] he was the first lichenologist to document Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:01:40, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282912000631 78 THE LICHENOLOGIST Vol. 45 in detail the fungal incorporation of cyano- mycobiont responds with different morpho- bacteria into the thallus. In a study on the logical structures to the relationship with cephalodia of Lobaria linita (Ach.) Rabenh., both photobionts. In the case of the foliose Winter reported that hyphae of the upper or lichen Lobaria pulmonaria (L.) Hoffm., the lower cortex grow towards adjacent cyano- green alga fill the dominant thallus and are bacteria colonies and expand between the situated in a layer directly below the cortex blue-green cells enveloping them. Forsell in the upper medulla, whereas the Nostoc (1884) supported this developmental process cells are found in cephalodia, which are but interpreted this association as a symbiotic attached to distinct parts of the thallus. In relationship. Observations of Hue (1904), photosymbiodemes, composed of green- Moreau (1921) and Kaule (1932) on cepha- algal and cyanobacterial sectors in the same lodia of the Lobariaceae are concordant with thallus, the cyanobacterial area is more ap- these authors. In contrast, Jordan (1970) pressed to the trunk in contrast to the green- found that cephalodia of the genus Lobaria algal parts. This morphological arrangement can only begin formation on the lower cortex. may be caused by the ecological need of He understood superior cephalodia as erum- the blue-green photobionts for liquid water pent bulbs that have grown through the thallus to be photosynthetically active (Green et al. from the lower to the upper cortex. 2002). A direct physical contact has never In cephalodia-forming lichens, the func- been observed between cyanobacteria and tional photosynthetic partner is a eukaryotic green algae (Rai & Bergman 2002). green alga, while the prokaryotic blue-green A further aspect of the tripartite life form photobiont fixes atmospheric nitrogen which is the role that cyanobacterial nitrogenous is used by both symbionts. Cyanobacteria in triggers may play in morphogenesis. Stocker- cephalodia have been shown to have higher Wo¨rgo¨tter (1994, 1995, 2001) found in re- heterocyst frequencies and higher rates of synthesis experiments of different photosym- nitrogen fixation than those in bipartite cyano- biodeme species that the growth of a new lichens (Rai & Bergman 2002). This nitrogen- thallus of Peltigera leucophlebia (Nyl.) Gyelnik fixing ability of cyanobacteria has two effects is initiated from a prothallus with Nostoc as on the lichen ecology. On the one hand, lichen the exclusive photobiont and young green species hosting N2-fixing cyanobacteria sym- lobes grow either on a cyanobacterial layer bionts show higher organic nitrogen concen- or on cyanobacterial lobules only. Similar trations compared to species without cyano- experiments with Lobaria fendleri (Tuck. & bacteria (Lawrey 1986). Consequently, Bu¨del Mont.) Lindau revealed that the green-algal & Scheidegger (1996) conclude that cyano- stages developed independently of the pres- bacterial lichens may have an advantage to ence of cyanobacteria, but stopped growing colonize special ecological niches, such as after one year. Sundberg et al. (2001) re- extremely oligotropic habitats. On the other moved cephalodia from Nephroma arcticum hand, in oldgrowth forests with high lichen (L.) Torss. and Peltigera aphtosa (L.) Willd. biomass, decomposition of cyanobacterial during four summer months and investi- lichens may contribute significant amounts gated the relationship between growth and of organic nitrogen to the forest ecosystem nitrogen concentrations. It might be that (Green et al. 1980; Guzman et al. 1990; cephalodia did not influence the lichen Knops et al. 1991; Antoine 2004; Knowles weight gain, the thallus growth on an area et al. 2006; Benner et al. 2007). basis was significantly inhibited. Observa- Although in recent years significant re- tions from Placopsis pycnotheca I. M. Lamb, search has been done on the interactions be- a primary colonizer of bare soils, showed tween mycobiont and photobiont (Honegger that its hypothallus formed cephalodia before 2001), less is known about the impact of formation of the typical squamules contain- both photobionts on the fungal phenotype. ing the green-algal photobiont (De los Rı´os It is evident that, on the same thallus, the et al. 2011). Downloaded from https:/www.cambridge.org/core. University of Basel Library, on 11 Jul 2017 at 09:01:40, subject to the Cambridge Core terms of use, available at https:/www.cambridge.org/core/terms. https://doi.org/10.1017/S0024282912000631 2013 Cephalodium formation in Lobaria pulmonaria—Cornejo & Scheidegger 79 Cephalodia are found in about 520 species Specimens were cleaned thoroughly in tap water, cut distributed through 21 genera (Hawksworth into small strips and immediately fixed in a 2% glutaral- dehyde phosphate buffer solution, pH 7Á1, for 2 h at & Hill 1984). They occur regularly in the room temperature. To wet the gas-filled cavities in the Stereocaulaceae and in the genera Psoroma medulla, flasks were evacuated carefully until the speci- and Placopsis, and they are also found fre- mens were completely saturated by the solution. After quently in the Peltigeraceae and Lobariaceae washing the specimens twice in phosphate buffer for 1 h (Henssen & Jahns 1974). It has been shown each, they were dehydrated in a water-ethanol series (30, 50, 70, 90 and 2 Â 100% ethanol puriss, 1 h each series). that cephalodia evolved independently in li- After dehydration, the specimens were infiltrated with a chens representing different systematic groups 1:1 ethanol-methacrylate mixture (Technovit, Kulzer) (Rikkinen et al. 2002; Lohtander et al. 2003; first for 4 h, then for
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