Botanical Journal of the Linnean Society (1988), 96: 3-20. With 18 figures
The variety of fungal-algal symbioses,
their evolutionary significance, and the
nature of lichens
D. L. HAWKSWORTH, V.-P.L.S.
CAB International Mycological Institute, Ferry Lane, Kew, Surrey TW9 3AF
Received February 1987, accepted for publication August 1987
HAWKSWORTH, D. L., 1988. The variety of fungal-algal symbioses, their evolutionary
significance, aad the nature of lichens. Symbioses between fungi and algae (or cyanobacteria)
can involve two-, three-, four-, five-, or more bionts. The range of symbioses developed is described
by means of examples with an emphasis on mutualistic symbioses. Lichen associations appear to be
very ancient and a study of the fungi in them is important to an understanding of ascomycete
evolution. An unequivocal definition of 'lichen' cannot be devised as fungi appear to be repeatedly
evolving and devolving with respect to forming mutualistic symbioses with algae, and strategies
may vary with age or be facultative. A revised definition to exclude 'mycophycobioses' is proposed,
and the terms 'phycotype' and 'parasymbiont' are rejected. A new combination in the genus
Pyrenocollema is made.
ADDITIONAL KEY WORDS:-Ascomycotina - Basidiomycotina - Deuteromycotina - coevolution - Cyanobacteria - Pyrenocollema.
CONTENTS
Introduction .
Two-biont symbioses
Mycobiont as inhabitant
Mycobiont as exhabitant
Three-biont symbioses .
Two photobionts: one mycobiont
Two mycobionts: one photobiont
Four-biont symbioses .
Three photobionts: one mycobiont.
Two photobionts: two mycobionts .
Three mycobionts: one photobiont.
Five- or more biont symbioses? .
Evolutionary significance .
Towards a definition of 'lichen'.
Acknowledgements
References.
3
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5
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8
II
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13
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14
16
17
17
INTRODUCTION
The range and complexity of symbioses* between fungi and algae (or
cyanobacteria) is staggering. In the last 10 years many fascinating cases have
*'Symbiosis' is used here in the original sense of de Bary (1879) to refer to different organisms Jiving
together, whether in mutualistic, commensalistic, or antagonistic associations. This practice is in accord with
that advocated by Starr (1975) and adopted by Cooke (1977), Ahmadjian & Paracer (1987), and Smith &
Douglas (1987).
3
0024-4074/88/010003+ 18 $03.00/0
©
1988 The Linnean Society of London
D. L. HAWKSWORTH
+
been brought to our notice which collectively both contribute to the century-old
debate as to the nature of lichen associations, and provide indications as to their
evolutionary significance.
In mutualistic : biotrophic) symbioses there is a stable relationship in which
both partners benefit; in commensalistic symbioses one partner benefits but the
other is not adversely affected or benefited; and in antagonistic (parasitic,
necrotrophici symbioses one partner benefits at the expense of the other which it
often kills. These categories are not exclusive; the biological relationship may
change with time from antagonistic to mutualistic, additional organisms such as
bryophytes may be an integral part of the symbiosis, and rarely have the
physiological, nutritional, and ultrastructural relationships been investigated.
I ndi\'idual fungal genera may even include species which are lichenized or not
sec p.l5 . It is therefore only practical to discuss symbioses in terms of the
number of participating organisms, or 'bionts' (Table 1). Poelt (1977) expressed
these in terms of two-, three-, or four-'membered symbioses'; 'biont' is adopted
here to confi)rm with 'mycobiont' (fungal partner; Scott, 1957) and
'photobion t' 1 photosynthetic partner; .·\hmadjian, l982a).
T\\'0-BIO:\'T
SY~IBIOSES
In mutualistic symbioses involving a single mycobiont and one photobiont,
either partner may be the 'inhabitant' living partly or wholly inside the other,
the 'exhabitant' ;Law & Lewis, 1983). The numerous antagonistic symbioses
where fungi are clearly parasitic on algae are not considered here; for further
information on these see Jones il976; and Kohlmeyer & Kohlmeyer ( 1979). ·
J(vcobiont as inhabitant
The classic case of a mutualistic situation in which the mycobiont is the
inhabitant or ·endophyte', is J~vcosphaerella ascopkvlli Cotton on the brown
TABLE l. The rangt' of fungal-algal symbioses in\'ol\'ing different numbers of bionts
:'\urn lwr of bioms
Examples
·1 \vo-biont snn bioses
\I Ycohiout .ts inhabitam
~I yrophycobioses
~h-robiont
.ts
~xhabitam
Thn·<·-biom <Ymbioses
T'"> photoi>ionts: one rnyrobiont
I'" o m\·robionts: one photobiont
Fungal parasites of algae
Lirhens
Cephalodia
Blue-green/green morphotypes
Algicolous lichens
Bryophilous lirhens
Lichmicolous fungi
~lerhanical hybrids
Four-biont svrnbioscs
Three photobionts: one myrobiont
T"·n photobionts: two mycobionts
Three rn\Tobionts: one photobiont
Cephalodia
Lichcnicolous lichens
Fungi on lichenicolous fungi
FiH·- or more biont symbioses
~lechanical
hybrids
FUNGAL-ALGAL SYMBIOSES
5
seaweeds Ascophyllum nodosum (L.) Le Jolis and Peluetia canaliculata (L.) Dcne &
Thuret (Smith & Ramsbottom, 1915; Webber, 1967; Kolhmeyer & Kolhmeyer,
1972). The ascomata form mainly in the receptacles of the algae (Figs 1, 2) and
the hyphae of the mycobiont ramify through the algal tissues (Fig. 3).
Uninfested algae do not appear to survive in nature (Webber, 1967), but the
physiology of the symbiosis remains obscure (Kingham & Evans, 1986). The
algae reproduce sexually, and, contrary to the general theory of Law & Lewis
(1983), the mycobiont forms both ascospores and conidia (spermatia) at the
surface of the algal fronds; this suggests the symbiosis is relatively recent in
origin and the selective pressure for the loss of sex is not strong in this instance.
A similar situation is suspected in the case of M . apophlaeae Kohlm. on the red
algae Apophlaea lyallii Hooker fil. & Harvey and A . sinclairii Harvey, forming
circular crustose thalli with concentric growth rings (Kohlmeyer & Hawkes,
1983).
Kohlmeyer & Kohlmeyer ( 1972) introduced the term ‘mycophycobiosis’ for
mutualistic associations in which the alga retained its form and continued to
reproduce sexually. However, in the symbiosis between Kohlmeyera complicatula
(Nyl.) Schatz (syn. Mastodia tessellata auct.) and species of the green algal genus
Prasiola (C. Agardh) Menegh., which they also treated as a ‘mycophycobiosis’,
the mycobiont appears to have a greater influence on the form of the alga
(Brodo, 1977; Kohlmeyer & Kohlmeyer, 1979). The Turgidosculum ulvae (Reed)
Kohlm. & E. Kohlm. and Blidingia minima (Naegeli ex Kutz.) Kylin association,
however, is closer to the Mycosphaerella ascophylli case, as is that between the
hyphomycete Blodgettia confervoides Harvey and species of Cladophora Kutz.; in the
latter case the hyphae are arranged in a roughly parallel manner within the cell
walls of the photobiont (Kohlmeyer & Kohlmeyer, 1979; Feldmann, 1938;
Hawksworth, 1987a). In the comparable association between Phaeospora lemaneae
(Cohn ex Woronin) D. Hawksw. and filamentous freshwater red algae
belonging to Lemanea Bory, both partners continue to reproduce sexually
(Hawksworth, 1987a).
It must be more than coincidence that all the above examples occur in sites
subject to periodic submersion. The presence of a mycobiont may therefore have
an as yet unidentified key role in reducing the physiological effects of water
stress and so enhancing survival. These examples may be recapitulating the
process of the colonization of land by progenitors of vascular plants (Pirozynski
& Malloch, 1975).
Mycobiont as exhabitant
Mutualistic symbioses in which the mycobiont is the sexually reproducing
exhabitant and the photobiont is a cyanobacterium or an alga with repressed
sexual processes encompass almost all taxa unquestionably accepted as lichens
by biologists. However, the 13 500 species of fungi exhibiting this life-style are
drawn from diverse systematic groups and display a range of complexity from
scarcely modified bionts to dual thalli substantially different from either partner
when growing alone.
The structurally simplest associations appear to be somewhat casual, as in the
bark-inhabiting genera of the Arthopyreniaceae; most species in that family are
not associated with any algae (e.g. Mycomicrothelia melanospara (Hepp) D.
6
D. L. HAWKSWORTH
FUNGAL-ALGAL SYMBIOSES
7
Hawksw.), some occasionally have small patches of Trentepohlia Harvey (e.g. M .
atlantica D. Hawksw. & Coppins), while others are constantly lichenized (e.g.
M . thelena (Ach.) D. Hawksw.) (Hawksworth, 1985a). In this family, the
ascomata and hyphae are intimately mixed with the bark tissues, and the fungi
involved can be expected to derive nutrients saprobically from the bark, in
addition to any that may be transferred from any photobiont present.
Loose symbioses with cyanobacteria or algae not leading to any specialized
morphological structures are seen in diverse fungi, for example: Acrospermum
adeanum Hohnel (Dobbeler, 1979), Chadefaudia corallinum (Crouan & P. Crouan)
E. Muller & v. Arx (Kohlmeyer, 1973), ‘Coniosporium’ aeroalgicola Turian
(Turian & Reymond, 1980), Cudoniella brasiliensis Rizz. (Rizzini, 1952),
Herpotrichia juniperi (Duby) Petrak (Moser-Rohrhofer, 1975), Orbilia luteorubella
(Nyl.) P. Karsten (Benny, Samuelson & Kimbrough, 1978), Pezizella parasitica
Velen. (Hawksworth & Sivanesan, 1976), Pseudotrametes gibbosa (Pers.) Bond. &
Singer (Wright, 1890), and Tricharina cretea (Cooke) Thind & Waraitch
(Benkert, 1981). In the associations between cyanobacteria and Didymella
lenormandii Henssen (Henssen, 1963), ‘Endomyces’ scytonematum Zukal (Zukal,
1891) , Nectria phycophila Zukal (Zukal, 1891), Phycorella scytonematis Dobb.
(Dobbeler, 1980), and Pyrenothrix nigra Riddle (Tschermak-Woess, Bartlett &
Peveling, 1983), the fungi are only known in the presence of particular
photobiont genera but no specialized morphological structures are formed. The
cryptoendolithic associations beneath the surface of rocks in Antarctica are
exceptionally specialized, but the bionts are again intimately intermixed with no
specialized tissues and the algae are associated to varying degrees (Freidmann,
1982). Some species of Epigloea Zukal produce a more thallus-like structure, but
without a differentiated cortical layer (Dobbeler, 1984). Zukal ( 1891) referred
to such associations as half-lichens (“Halbflechten”) .
The mycobiont ensheaths the photobiont filaments in Coenogonium Ehrenb. ex
Nees, Cystocoleus Thwaites (Fig. 4), Dictyonema moorei (Nyl.) Henssen
(Tschermak-Woess, 1983), Ephebe Fr., and Racodium Fr. but the morphology of
the photobiont is scarcely modified. However, in Strigula elegans (Fke) Mull. Arg.
as colonies of the alga Cephaleuros virescens Kunze are lichenized, sporangiospore
production is repressed and the thallus form is modified by the mycobiont
(Ward, 1884); a parallel situation occurs with foliicolous Porina Mull. Arg.
species and algae belonging to Phycopeltis Millardet. In the production of
unlayered Collema Wigg. thalli, Nostoc Vaucher ex Bornet & Flah. colonies are
modified by the mycobiont ramifying through them but this is unable to
comdetelv determine the overall structure and the Dhotobiont cells remain
dispkrsed ihrough the thallus and not in a differentiatid layer (Degelius, 1954;
Fig. 6).
I n contrast, in the majority of cases with mycobionts from exclusively or
predominantly lichenized orders (e.g. Graphidales, Gyalectales, Lecanorales,
V
I
Figures 1-8. Two-biont symbioses. Figs 1-3. Mycosphaerella ascophylli. Fig. 1. Lobe tip with
ascomata, x 170. Fig. 2. Vertical section of ascoma, x 270. Fig. 3. Vertical section of thallus
showing mycobiont hyphae ramifying between the cells of the photobiont, x 270. Fig. 4. Cystocoleus
ebeneus (Dillw.) Thwaites, showing septae of Trentepohlia and ensheathing mycobiont hyphae, x 430.
Fig. 5. Lecidella elaeochroma (Ach.) M . Choisy, vertical section, x 270. Fig. 6. Collema auriforme
(With.) Coppins & Laundon, vertical section, showing dispersed Nostoc cells, x 170. Fig. 7. Parmelia
saxatilis (L.) Ach., vertical section showing localized Trebouxia cells, x 270. Fig. 8. Bryoriafuscescens
(Gyelnik) Brodo & D. Hawksw., transverse section showing localized Trebouxia cells, x 270.
D L HA\$KS\VORIH
8
Opegraphales. Peltiger ales, Teloschistales), the mycobiont appears to have the
ke) role i n determining thallus form. The inhabiting photobiont is generally
limited t o a well-defined layer within the thallus, whether that is crustose
‘Fig. 5 , foliose Fig. 5 ) or fruticose (Fig. 8 ) . T h e great range of morphological
complexit1 may be attributable to the mycobiont striving to achieve the shape
most conducive to displaying the maximum area of photobiont cells to light,
and so impro\e its fitness and ability to spread into otherwise hostile
en\ironmcnts.
In pure culture mjcobionts rarely produce colonies reminiscent of the
compo5ite thallus (Ahmadjian, 1967). The complex dual structures found in
nature arc a consequence of an interaction between the bionts in which the
m j cobiont ha5 the dominant role and influences the distribution of the
photobiont cells (Grecmhalgh & Anglesea, 1979). Further, single mycobionts
( an produce similar thalli (with identical secondary metabolites) with different
afgae, for example either Trebouxza albulescens de Nicola & Bened. or 7.
decolorans
.lhm. in .Yanthorza parzetzna (L.) T h . Fr. (Piatelli & de Nicola, 1968), and
. J h hocorcu, Naegeli or ‘Trebouuza Puymaly in Chaenotheca carthusiae (Harm.) Lettau
Iihell, 1982). However, the same photobiont species may occur with a variety
of mFcobiont genera (e.g. Hildreth & Ahmadjian, 1981).
O t t 1987ai has found that X . parzetzna associates with foreign algae in the
c‘drli stage5 of de\Jelopment as a stop-gap prior to contact with an appropriate
Trehourza species and subsequent thallus differentiation.
Differences in thallus colour in Peltzgera polydactyla (Necker) Hoffm.
0 I’itikainen, unpublished data) and Stzcta caulescens de Not. (D. J. Galloway
& P. \V. *James, unpublished data) have also been attributed to their
m>cohiont\ associating with different cyanobacteria.
IYhether lichen associations are truely mutualistic has often been questioned
(Smith, 19751; indeed some authors assert that the photobiont is parajitiLed b) the m) cobiont ( Ahmadjian, 1982b; Ahmadjian & Jacobs, 1983).
A 5 the m>cobiont is generally only able to survive with the photobiont, and as
the photobiont debelops in environments where it could not survive alone, the
s\mhiosis has to he viewed as mutualistic. In considering the ‘benefits’ to the
photobiont it is crucial to consider the fitness of populations and not individual
cells. parallel situations are familiar to sociobiologists as ‘altruism’ (e.g. Barash,
1977 .
T H R E E - B I O S ’ I SYMBIOSES
Two photobionts: one mycobiont
1he most easily recognized cases of mutualistic symbioses involving two
photobionts and a single mycobiont involve both a green alga and a
ryanobacterium. These occur in about 500 species dispersed through some 20
genera in five orders i James & Henssen, 1976). One of the photobionts may be
contained in a separate internal layer in the thallus (e.g. Solorina crocea (L.) Ach.;
Fig. 9 ! , as scattered internal packets (e.g. Lobaria pulmonaria (L.) Hoffm.) or in
external morphologically distinct structures (‘cephalodia’). The latter vary from
modified lobes (e.g. Placopsis gelida i L.) Lindsay) through convex swellings (c.g.
Peltigera aphthosa i L.) h’illd.; Fig. lo), to leaf-like (e.g. Sticta canariensis (Ach.)
Kor)~ ex Delise, S. Jilix (Rausch.) Nyl.; Fig. 1 1 ) or shrubby outgrowths (e.g.
? _
FUNGAL-ALGAL SYMBIOSES
Figures 9-16. Three-biont symbioses. Fig. 9. Solorina crocea, vertical section showing two layers with
different photobionts, x 170. Fig. 10. Peltigera aphthosa, vertical section of 'cephalodium' containing
cyanobacteria on an algal-containing thallus, x 170. Fig. II. Sticta.filix, showing foliose green-algal
morph (arrow) arising from the fructicose cyanobacterial morph, x 2. Fig. 12. Polycoccum galligenum
Vezda, forming galls on Physcia caesia, x 25. Fig. 13 . .Nesolechia oxyspora bleaching thallus of Parmelia
saxatilis, x 15. Figs 14-15. Vezdaea aestivalis. Fig. 14. Habit on moss leaves. X 5. Fig. 15. Vertical
section of moss h~af showing the subcuticular algal cells, x 170. Fig. 16 . .Nectria phycophora, surface
view of ascoma showing groups of algal cells in pockets of the ascoma wall, x 430.
0
D. L. HAWKSWORTH
Ill
Lobaria amplissima (Scop.) Forss.). In Psoroma durietzii P. James & Henssen the
cephalodia become sorediate and form independent cyanobacterial thalli, which
in turn may capture green algae (James & Henssen, 1975).
The production of morphologically distinct structures with cyanobacteria, as
opposed to algae, is of especial interest in emphasizing that the resultant thallus
is a result of the interplay between the bionts. Algal and cyanobacterial
morphotypes* may be found joined together or as independent two-biont thalli.
They have often been given separate scientific names, and new cases of
connected thalli are repeatedly coming to light (Brodo & Richardson, 1978;
Renner & Galloway, 1982; T0nsberg & Holtan-Hartwig, 1983).
The second photobionts are captured from nature, and then progressively
incorporated into the thallus (Jordan & Rickson, 1971). The microenvironment appears to have a key role in determining whether independent
two-biont thalli develop, as described, in Stictafilix (James & Henssen, 1976). In
nutrient-poor habitats the ability to incorporate a nitrogen-fixing
cyanobacterium as a third biont increases the fitness of the original two-biont
symbioses.
A different three-biont situation exists in Pyrenocollema pelvetiae (SutherI.) D.
Hawksw.t where the mycobiont and associated cyanobacteria grow
epiphytically on Pelvetia canaliculata (Kohlmeyer, 1973; Kohlmeyer &
Kolhmeyer, 1979). This is perhaps most appropriately referred to as an
obligately algicolous lichen-i.e. a mutualistic symbiosis in a commensalistic
symbiosis, as the Pelvetia is presumably not advantaged. 'Pharcidia' laminariicola
Kohlm. and 'P.' rhachiana Kohlm., both on Laminaria digitata (Huds.) Lamour.,
are similar algicolous lichenoid associations (Kohlmeyer, 1973; Kohlmeyer &
Kohlmeyer, 1979).
At least 19 lichen-forming genera include species exclusively associated with
bryophytes (Poelt, 1985a). The degree of specificity varies, but many are
confined to particular mosses or liverworts and must be regarded as parasitic,
eventually killing the host. The thalli are generally superficial but some persist
in a commensalistic symbiosis in which the algal or cyanobacterial partner
grows below the cuticle of the moss leaves. In Vezdaea aestivalis (Ohl.) Tsch.\Voess & Poelt the Leptosira obovata Vischer chlorococcalean photobiont is
sustained subcuticularly on living bryophyte leaves for some time before they die
(Tschermak-Woess & Poelt, 1976; Figs 14-15). No mycobiont cortex is
differentiated in this case, nor in the hyphomycete Velutipila poeltii D. Hawksw.,
also associated with chlorococcalean algae and moss leaves (Hawksworth,
1987a). In Arthopyrenia endobrya Dobb. & Poelt, Trentepohlia filaments and the
mycobiont both develop together inside the leaf cells of hepatics (Dobbeler &
Poelt, 1981); in Porina heterospora (Fink) R. C. Harris the mycobiont hyphae
envelop and penetrate moss leaf cells (P. W. James, unpublished data); and in
"Vectria phyrophora (Dobb.) Rossman, on leaves of Dawsonia grandis Schlieph. &
*This term is used here in preference to 'phyrotype' ISwinscow, 1977) and other terms proposed (Tunsberg
as the photosynthetic partner may be either an alga or a cyanobacterium.
\forphological variants caused by different photobionts can be denoted by, for example, 'blue-green
rnorphotvpe' or ·Coaomyxa-morphotype' when this is desirable. If a new separate term is considered necessary
'phototvpe' would be one possibility. but this has been used in the printing industry since lR.'i9.
& Holtan-Hartwig. 1983
+PyrenocollenuJ pelvetiiUl ,:Suther!., D. Hawksw .. comb. nova.
Transactirms
'!f the
British
.\~ycological
Society, 5: 15 7 r 1915 , .
BASIONYM:
Dothidella pelvetiae Suther!.,
FUNGAL-ALGAL SYMBIOSES
11
Geh., algal cells occur in circular depressions in the ascoma wall (Dobbeler,
1978; Fig. 16).
Although the bryophyte partner in such three-biont symbioses is often
naturally short-lived, it seems unlikely that it would be placed at any advantage
by the additional bionts. I therefore agree with Poelt (1985a) that such
associations should be regarded as parasitic bryophilous lichens, even when they
can develop only in the presence of an appropriate- bryophyte. These
associations can be compared to subcuticular foliicolous lichens on phanerogam
leaves in the tropics where the supporting leaves continue to photosynthesize
and are not killed (Hawksworth, 1987b).
Two mycobionls: one photobiont
The lichenicolous fungi, some 300 genera and 1000 species, exhibit a variety
of biological relationships with their host two-biont mutualistic symbioses. These
range from parasitic to commensalistic*, or even mutualistic and saprophytic
(Hawksworth, 1982a). Parasitic symbiotic fungi may cause extensive damage
leading to thallus death (e.g. Athelia arachnoidea (Berk.) Julich, Lichenoconium
erodens M. S. Christ. & D. Hawksw., Nectriella santessonii Lowen & D. Hawksw.,
Nesolechia oxyspora (Tul.) Massal.; Fig. 13) or form localized necrotic patches (e.g.
Cornutispora lichenicola D. Hawksw. & B. Sutton, LPhragmonaevia’ peltigerae (Nyl.)
Rehm).
In commensalistic lichenicolous fungi an additional mycobiont co-exists with
the existing mutualistic symbiosis, presumably sharing the products of the
photobiont either directly or indirectly but not damaging or benefiting the host
mutualistic symbiosis. Amongst numerous examples (see Hawksworth, 1983) are
Arthonia glaucomaria (Nyl.) Nyl. (on Lecanora rupicola (L.) Zahlbr.), Skyttea cruciatu
Sherw., D. Hawksw. & Coppins (on Diploicia canescens (Dickson) Massal.),
Sphinctrina turbinata (Pers.) de Not. (on corticolous Pertusaria DC. species), and
Weddellomyces epicallopismum (Weddell) D. Hawksw. (on placodioid Caloplaca
Th. Fr. species). In other instances gall-like growths are produced as a result of
the interaction, as in Bachmanniomyces uncialicola (Zopq D. Hawksw. (on Cladonia
unciulis (L.) Wigg., etc.) , Guignardia olivieri (Vouaux) Sacc. (on Xanthoria
parietina) , Plectocarpon lichenum (Sommerf.) D. Hawksw. (on Lobaria pulmonaria
(L.) DC.), Polycoccum galligenum VEzda (on Physcia caesia (Hoffm.) Fiirhohr;
Fig. 12); and Thamnogalla crombiei (Mudd) D. Hawksw. (on Thamnoliu Ach. ex
Schaerer). The morphogenetic and physiological processes in these cases are
obscure and promise to be a fascinating area for innovative research.
A modification of the lichenicolous habit is seen where a mycobiont initially
parasitizes an existing dual association, progressively eliminates the primary
mycobiont, and takes over the photobiont to produce a mutualistic thallus of its
own. This phenomenon is probably more widespread than is generally assumed,
and further examples are being discovered at an increasing rate now that
lichenologists are aware of it. Selected instances are Arthrorhphis citrinella (Ach.)
Poelt (on Baeomyces rufus (Huds.) Rebent.), Blarntya hibernica D. Hawksw.,
Coppins & P. James (on Enterographa Fie and Lecunactis Eschw.), Diploschistes
*Lichenicolous fungi not damaging their hosts and persisting on them have long been termed
‘parasymbionts’ (Zopf, 1897). However, with the broader concept of ’symbiosis’ now accepted (see p. 3), this
term becomes superlluous and such fungi are more appropriately referred to as ‘commensalistic’.
12
D. I,. HAiVKS\YORI H
cnasiop1urnbuu.i (Xyl.i Vainio ( o n Lecanora gangaleoides Nyl.; Fig. 17), Lecanora
praepostera S y l . ion Aspicilia epzghpta (Norrlin ex Nyl.) Hue), and Lecidea insidiosa
‘Th. Fr. (on Lecanora uarza (Hoffm.) Ach.). In Chaenothecopsis consociata (Nadv.) A.
Schmidt on Chnenotheta cizr_vsorephaln iTurncr ex Ach.) T h . Fr.), Tschermak-
k’igurrb I iV18. k’our-thnt symbioses. Fig. I i . 1)iplusrhistr.r raesioplunzbeuJ parasitic
011 Leranura
,pn,yolroid~s.showing the whitish nccrotic zone of dcad Lerunora tissue at the margin of the growing
DiploschiJfrs thallus, x 1.5. Fig. 18. Lecidra insulurk commerisalistic on Lecunoru rupirolu, note the
;ibcenw of 3 nccrotir zone on the Lrmnorn, x 3.5.
FUNGAL-ALGAL SYMBIOSES
13
Woess ( 1980) discovered that the Chaenotheca’s Trebouxia simplex Tsch.-Woess
photobiont was later replaced by Dictyochloropsis symbiontica Tsch.-Woess, and in
D . muscorum (Scop.) R. Sant. (on Cladonia Hill ex Browne), Fried1 (1987) found
that the Cladonia’s photobiont, Trebouxia irregularis Hildr. & Ahm., was used
initially but subsequently preferentially exchanged for 1.showmanii (Hildr. &
Ahm.) Gartner. It is conceivable that several of the lichenicolous lichens
discussed below start in a parallel manner.
Some of the ‘mechanical hybrids’ formed by fusion of propagules may also
belong in the three-biont category, but as these can involve more bionts they are
considered separately below (p. 14).
FOUR-BIONT SYMBIOSES
Three photobionts: one mycobiont
This situation is conclusively reported in Nephroma arcticum (L.) Torss. where a
thallus was found to include two morphologically distinct cyanobacteria in
separate internal patches in addition to the principal Coccomyxa Schmidle
photobiont (Jordan & Rickson, 1971). Parallel cases may occur in Peltigera
Willd.; Brodo & Richardson (1978) illustrate a thallus of P. aphthosa with a
Nostoc which supports Coccomyxa-containing lobules which in turn have Nostoccontaining excrescences.
While instances involving three photobionts easily distinguished
morphologically appear to be rare, it is probable that parallel situations
involving photobionts of the same genus are much more frequent than is
generally supposed (see p. 16).
Two photobionts: two mycobionts
Examples involving two photobionts each associated with a separate
mycobiont are seen in the obligately lichenicolous lichenized fungi. This
biological group has not been given the attention it merits in view of its
widespread occurrence. Poelt & Dopplebaur (1956) listed 100 lichenicolous
lichenized species, but the actual number is probably higher by a factor of two
or three.
In contrast to cases such as Diploschistes where one fungus initially parasitises
an already lichenized thallus (see p. 12), the lichenicolous lichens maintain a
separate photobiont, often in a conspicuous thallus, as in Lecidea insularis Nyl.
(on Lecanora rupicola: Fig. 18), Verrucaria aspiciliicola R. Sant. (on Aspicilia calcarea
(L.) Mudd) and species of Acarosfora Massal. (Poelt & Steiner, 1972), Caloplaca
Th. Fr. (e.g. C. epithallina Lynge on 13 hosts; Poelt, 1985b) and Rhizocarpon
Ram. ex DC. (Poelt & Hafellner, 1982; Holtan-Hartwig & Timdal, 1987). In
Xanihoria parietina, photobiont cells can be extracted from adjacent thalli of
Physcia tenella (Scop.) DC. (Ott, 1987a).
In Buellia badia (Fr.) Massal. (on Parmelia annexa Kurok. and P. verruculifera
Nyl.) , B. puluerulenta (Anzi) Jatta (on Physconia distorta (With.) Laundon;
Hafellner & Poelt, 1980), and Rhizocarpon uorax Poelt & Hafellner (on Pertusaria;
Poelt & Hafellner, 1982) the thallus of the lichenicolous lichen remains covered
by the cortex of the host. Several other cases which may fall into this category
D. L. HALVKSWORTH
I4
require further study :e.g. Candelariella superdislans (Nyl.) Malme on Lecanora
distans (Pers.) Nyl.).
As the fitness of the host in all these cases is presumably not increased, such
symbioses are appropriately regarded as commensalistic or parasitic lichens.
Three myrobionts: one pholobionl
This evidently extremely rare situation may occur in the association between
the hyphomycete Trichoconis lichenicola D. Hawksw. and galls caused by the
ascomycete Pvrenidium artinellum Nyl. on Peltigera collina (Ach.) Schrader
[Hawksworth, 1980).
FIVE- OR MORE BIOS?’ SYMBIOSES?
v ,
l h a t associations including five or more bionts exist in nature now seems
highl) probable. These may arise through the production of ‘mechanical
hybrids’ 1 Hawksworth, 1978) in which bionts from different propagules grow
together to form a single structure. This phenomenon, whose fundamental
importance was stressed by Bowler (1976), and which was first documented in
Cladia Nyl. (Jahns, 1972), could explain some complex thalli in Alectoria Ach.
(Brodo, 1978), and has been elegantly demonstrated by scanning electron
microscopy in Hypogymnia physodes (L.) Nyl. and Usnea Jilipendula Stirton
‘Schuster. 1985), and Physcia adscendens (Fr.) H. Olivier, P. tenella and Xanthorza
parietina. In the latter cases interspecific and intergeneric mechanical hybrids
have been documented (Schuster, Ott & Jahns, 1985; Ott, 1987b). Coalescence
of already established independent thalli is also documented, as in Lecanora
gangaleoidec Yyl. (Hawksworth & Chater, 19791, and is a possible cause of error
in lichenometry (Jochimsen, 1966).
In these, and other examples discussed by Jahns (1988), the asexunl
propagules growing together may be derived from the same parent thallus, in
which case the bionts may be genotypically identical ( i x . from the same clone).
However, Larson & Carey (1986) found that single large thalli of Umbilicurza
uellea (L.) Ach. and L:. mammulata (Ach.) Tuck. are not uniform with respect to
physiological parameters and isoenzyme profiles; young thalli appear to be
mainly monomorphic whereas older larger thalii are highly polymorphic. ‘I’heir
results are perhaps most plausibly explained by the ‘mechanical hybrid’
concept, supplementary mycobiont strains being incorporated with age.
Additional photobionts may be captured and integrated either by thalli
growing over them (Jordan & Rickson, 1971) or as a result of their alighting on
the thallus surface (Brodo & Richardson, 1978). Occurrences of this type could
rvell be frequent, but most will remain undetected until multiple isolates of
photobionts are cultured from single thalli.
E\’OLC‘I‘IOSARY SIGNIFICANCE
’fhe formation of mutualistic symbioses with photobionts, including forest
trees. orchids, endophytes of other vascular plants, liverworts, algae and
ryanobactcria, is so widespread amongst the fungi that this must confer a major
crdutionary advantage. At a conservative estimate, of the 64 200 species of
FUNGAL-ALGAL SYMBIOSES
1.5
fungi (Hawksworth, Sutton & Ainsworth, 1983) about 30% (19 000 species)
have adopted this habit: over 5000 (8%)as mycorrhizal (Malloch, Pirozynski &
Raven, 1980) and 13 500 (21yo)as lichen associations.
The distribution of the species entering into lichen associations amongst the
major groups of fungi is far from regular: 98% belong to the Ascomycotina, but
while 16 of the currently accepted 46 orders (Eriksson & Hawksworth, 1986)
include at least some lichenized representatives, only six are exclusively
lichenized. There are relatively few lichenized Hymenomycetes (e.g. Dicponema
C. Agardh ex Kunth., Multiclauula R. Petersen, Omphalina QuCIet p.p.), one
probably mastigomycete lichen (Geosiphon pynforrnes (Kiitz.) Wettst.) and about
50 genera of lichen-forming conidial fungi (Vobis & Hawksworth, 1981;
Hawksworth & Poelt, 1986); the latter almost all have affinities with the
Ascomycotina. Further, about 20 genera include both lichenized species and
ones with other nutritional modes (Hawksworth & Hill, 1984). The clear
impression is of an evolutionarily significant strategy which is currently evolving
in some fungi (e.g. Hymenomycetes, Helotiales) but devolving in others (e.g.
certain Caliciales and Lecanorales) .
The lichen life-style is very ancient, as suggested both by co-evolutionary
considerations (Hawksworth, 1982b, 1988) and phytogeographic studies relating
modern distributions to continental movements (Sheard, 1977; Sipman, 1983;
Tehler, 1983). It seems probable that many of the primarily lichenized families,
genera, and in some cases species and even chemotypes, evolved in PermoTriassic times around 190-280 Myr B.P., before the rise to dominance of the
phanerogams in the Cretaceous (65-136 Myr B.P.). In an attempt to display
the orders of the Ascomycotina as a whole in relation to their biology, it was
found that the Peltigerales came to occupy a somewhat central position (Dick &
Hawksworth, 1985). It is interesting that this order was also highlighted as of
possibly particular significance in ascomycete evolution on other grounds
independently by Eriksson (1981) and Hawksworth (1982b). Further, the order
includes some genera which are essentially terricolous, although able to spread
onto mossy bark and trees; i.e. with primary habitats which would have existed
before the rise of the phanerogams. Whether the habitats were determined by
the presence of suitable photobionts, or whether lichen associations facilitated
the colonization of habitats unsuited to the unprotected photobiont is a matter
for conjecture. It may also be relevant that in this group of lichens the
photobionts are regularly cyanobacteria; the cyanobacteria could have arisen in
the Precambrian, as far back as 3500 Myr B.P. (Walsh & Lowe, 1985) and so
would have been some of the first potential photobionts available for any
emerging fungi.
The extent to which present-day Peltigerales, or indeed certain other
anciently lichenized groups such as the Pertusariales and Teloschistales, retain
features of the earliest ascomycetes is open to debate. Nevertheless, it is clear that
such orders cannot be conveniently passed over by mycologists as they may
prove to be central to an overall interpretation of ascomycete phylogeny. A
failure to consider lichenized and non-lichenized groups together has been a key
factor in hampering the development of a satisfactory taxonomy for this, the
largest subdivision in the fungal kingdom (Hawksworth, 1985b).
In addition to the significance of the study of lichen-forming fungi for the
classification of the Ascomycotina as a whole, co-evolution has taken place
lb
D. L. HAWKSWORTH
bet\veen the bionts leading to novel morphologies, dual asexual reproductive
propagules, and secondary metabolites formed only in the combined thallus
!Ha\vksworth, 1988).
TOWARDS A DEH:\"IT10.11; OF 'LICHEN'
A consideration of the range of biological situations in fungal-algal symbioses
is a prerequisite to attempts to provide an unequivocal definition of the term
'lichen'. Ever since the dual nature of lichens became apparent in the 1860s,
biologists have struggled to produce generally acceptable forms of words:
... it is quite impossible to distinguish some lichens from fungi ...
Berkeley (in Lindsay, 1869)
... a fungus which lives during all or part of its life in parasitic relation
with the algal host and also sustains a relation with an organic or an
inorganic host.
Fink (1913)
... a fungus ... exclusively or sometimes living with, but not apparently
harming, an alga and which is studied by lichenologists.
Hawksworth ( 1978)
... an association of a fungus and an alga in which the two organisms are
so intertwined as to form a single thallus . . . Alexopoulos & Mims ( 1979)
... an association of a fungus and a photosynthetic symbiont resulting in a
stable thallus of specific structure.
Ahmadjian ( 1982c)
... a fungal--algal association which forms a thallus that does not resemble
either symbiont in the free-living ( = unlichenized) state.
Ahmadjian ( 1982d)
... a stable self-supporting association of a fungus (mycobiont) and an alga
or cyanobacterium (photobiont).
Hawksworth et al. (1983)
... associations between fungi as hosts and algae or cyanobacteria as
symbionts.
Smith & Douglas (1987)
The definition of Ahmadjian ( 1982c), based on discussions by a committee
and a subsequent poll of the International Association for Lichenology, is not
satisfactory as there is then a need to define a "thallus ofspecific structure". On
the basis of this definition, filamentous lichens such as Cystocoleus, some poorly
formed leprose and crustose thalli (e.g. certain Micarea Fr. species) and many
pyrenocarpous lichens immersed in bark or rock would be excluded. Debates
would continue over cases such as lvfycosphaerella ascophylli and Turgidosculum
ulvae (the 'mycophycobioses'), and more casual associations (see p. 5). The
description of the mycobiont as 'host' is inappropriate as the shape is a result of
the mutualistic association and in the case of filamentous lichens it is the
photobiont that has most claim to that title.
It is never likely to be feasible to produce a totally satisfactory definition in
the dynamic evolving and devolving situation which confronts us. However,
many lichenologists are keen to exclude mycophycobioses (and cases such as
Epigloea and Velutipila) which come within the definition of Hawksworth et al.
'1983). In these instances the photobiont is the exhabitant; the mycobiont
FUNGAL-ALGAL SYMBIOSES
17
hyphae ramify through the photobiont. If this important dichotomy is taken
into account, a more acceptable definition can be provided €or those still wishing
to treat ‘lichens’ independently in floristic and ecological investigations:
A lichen is a stable self-supporting association of a mycobiont and a
photobiont in which the mycobiont is the exhabitant.
It is important to emphasize that this definition does not represent a single
biological type of association. I n addition to mutualism with algae (or
cyanobacteria) being gained in some genera and lost in others, biological
strategies may be facultative or change with time. Biologists in general and
mycologists in particular need to recognize that a single definition which can
unequivocally categorize each mutualistic fungus-alga relationship discovered is
not achievable; where possible broader symbiological terminology should be
adopted.
There are numerous parallels between lichen symbioses and mycorrhizas in
their definition, classification, polyphyletic nature, structure, physiology, and
carbohydrate nutrition (Smith, Muscatine & Lewis, 1969; Harley, 1984; Lewis,
1987; Smith & Douglas, 1987). However, scientists working with mycorrhizas
have traditionally regarded themselves primarily as mycologists or foresters
rather than as mycorrhizologists. This has resulted in a broadly based and
integrated approach to those mutualistic associations. In contrast, the tendency
of students of lichens to regard themselves as lichenologists rather than as
mycologists or phycologists has resulted in an introspective approach which has
limited the development of our understanding of these biologically fascinating
symbioses, as already stressed by Santesson (1 967). Lichenologists are urged to
view themselves first as mycologists or phycologists. Conversely, mycologists and
phycologists require encouragement to integrate thoroughly lichens into their
teaching and research programmes to the extent justified by their variety and
numbers; they have much to contribute (Smith, 1978).
ACKNOWLEDGEMENTS
I am indebted to Mr P. W. James and Dr K. A. Pirozynski for their
comments and stimulating discussion of an early draft of this contribution; to
Miss G. Godwin for photographic assistance; to Mrs C. Thatcher for microtome
sections; and to Mrs M . S. Rainbow for word-processing.
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0
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