The genus Acantholichen was first described by Jørgensen (1998), who, at the time, considered the genus to be monotypic [Jørgensen (1998) Acantholichen pannarioides, a new basidiolichen from South America. Bryologist 101:444–447]. Specimens from the Galapagos, collected by Pike in Santiago (OSC), and by Weber and Lanier in Santa Cruz (COLO), were cited by Jørgensen in the protologue, alongside type material of Acantholichen pannarioides P.M. Jørg. from Costa Rica.
Dal-Forno et al. (2016) compared morphology and anatomy of specimens from Galapagos with those collected in Costa Rica, Brazil and Colombia; combined with a molecular analysis. In the genus they thus distinguished six different species, describing the material from Galapagos as Acantholichen galapagoenis Dal-Forno, Bungartz & Lücking, a species endemic to the archipelago [Dal-Forno et. al. (2016) From one to six: unrecognized species diversity in the genus Acantholichen (lichenized Basidiomycota: Hygrophoraceae). Mycologia, 108(1): 38–55].
This basidiolichen species is endemic to Galapagos. A recent species inventory found only five populations across four different islands. Natural habitats of Acantholichen are known from threatened tree ferns and shrub (Cyathea - endangered, Psychotria - vulnerable) and a vegetation type that is in many parts of Galapagos has deteriorated (Frullania-Zanthoxylon forests). Only on Santa Cruz thalli of the lichen have established on introduced Cinchona pubescens as an alternative habitat. Here, the practice of population reduction of Cinchona by chemical control needs to be carefully balanced against survival of refugium populations of Acantholichen.
Endemic to the Galapagos Islands, Ecuador. Known from the highlands of Isabela Island (Cerro Azul, Volcán Alcedo), Santiago, Santa Cruz, and San Cristóbal Island.
Acantholichen galapagoensis occurs at upper altitudes of the humid zone vegetation [typically from 650 to 900 m, min. 500m, max. 1100 m]. The species is known from only four islands (San Cristóbal, Santa Cruz, Santiago, Volcán Alcedo and Cerro Azul on Isabela). Despite intensive surveys it was not found on other islands that have a fairly well developed humid zone, like Floreana or Pinta. Even above 500 m altitude Acantholichen was not found on these islands, which generally lack open, exposed, but nevertheless extremely humid habitat.
Historic collections from Santiago by L.H. Pike (OSC), and Santa Cruz by W.A. Weber and J. Lanier (COLO) suggest that this endemic Galapagos basidiolichen was once common in the natural vegetation of the humid Galapagos highlands. On the four different islands, from which the lichen is today known, populations are all locally restricted, i.e., apart from the two main volcanoes of Isabela (Cerro Azul, Alcedo) each island can be considered to support only one distinct population [VU B1a; due to the close proximity of the five populations on the four islands, even EN B1a might apply].
Specimens on native and endemic trees and shrubs are today typically not well developed (listed as A. pannarioides during Galapagos Lichen Inventory: http://www.darwinfoundation.org/datazone/collections/). They are often reduced to few, scant squamules. This contrasts, however, with exceptionally well developed material growing on Cinchona pubescens, an introduced tree that invades shrubland dominated by endemic Miconia robinsoniana in the highlands of Santa Cruz Island. There, the lichen is particularly abundant on dead trees left standing from conservation management (chemical control of invasive Cinchona). In some instances the basidiolichen here covers up to 1 m length of the tree trunks. This refugium population on Cinchona is, however, known from a single location, the Miconia scrub invaded by Cinchona between El Puntudo and Cerro Crocker
Similarly well developed thalli are otherwise only known from Isabela Island (Cerro Verde, Volcán Cerro Azul), where thalli grow abundantly on leaf sheaths of the endemic tree fern Cyathea weatherbyana. Cyathea is listed as globally Endangered [EN A2a,c,e with its populations on Santa Cruz threatened by invasion of Cinchona and most other populations severely reduced by feral goats; only the Cerro Azul populations are assumed to be relatively stable].
Other native habitat is demonstrated by specimens found on the endemic Psychotria rufipes [VU B1a,b(iii,v); B2a,b(iii,v)] in the highlands of Santiago, and remnants of Frullania-Zanthoxylum forests (“brown zone”-vegetation), where Acantholichen grows on isolated Zanthoxylum snags along the outer caldera rim of Volcán Alcedo, Isabela Island.
The native lichen populations on Cyathea are likely to decline further, if populations of the tree fern continue to deteriorate. Currently, lichen populations established on Cinchona in Santa Cruz act as refugia, as long as dead tree stumps are not removed. Overall it can be assumed that these populations remain relatively stable under the current management regime (chemical control, without mechanical removal of dead trees).
However, in the past two years (2015-17) the terrestrial parts of the Galapagos have experienced very unusual and extreme droughts. In the highlands it barely rained during the rainy seasons, farmers started to complain that their cattle was dying from starvation because the otherwise abundant grasslands in the agricultural areas were drying up. During a visit to Santa Cruz for six weeks in February March of 2017 we witnessed these exceptionally dry conditions. Even the most humid parts of the highlands were now without clouds for weeks. The sphagnum bogs in the highlands felt dry, the Sphagnum plants dying off. During an intensive search for Acantholichen we were able to find only very few, scant squamules at the locality from which the most abundant populations were previously known. This suggests that under current abnormal climate conditions even the populations previously assumed to provide stable refugia are now declining.
Population Trend: Deteriorating
Acantholichen galapagoensis appears to be relatively substrate unspecific. It grows on hepatics (most commonly Frullania aculeata, less commonly on Frullania brasiliensis, Frullania sp., Ceratolejeunea sp., Omphalanthus filiformis). Two specimens from Santa Cruz were found on terricolous Campylopus anderssonii on open, exposed ground. Well developed thalli of the lichen were also found on dead leaf sheaths of the endemic tree fern Cyathea weatherbyana.
Despite its ability to inhabit a broad range of substrates the microhabitat of the basidiolichen nevertheless appears very restricted. Characteristic is a combination of factors that rarely occur together: open and exposed, but nevertheless almost continuously humid conditions.
The species has generally only been found in the most humid environments, in habitat that throughout the year are is constantly subjected to a fine drizzle or fog (locally known as ‘garua’). At the same time, in these environments Acantholichen inhabits only the most exposed, unsheltered sites that receive direct sunlight (sun-, wind- and rain-exposed); it does not occur within closed canopy; thalli are best developed where they are most exposed.
In Santa Cruz, for example, the lichen is not generally found throughout the humid highlands. Instead it is restricted to a relatively small area near El Puntudo and Cerro Crocker; a region typically shrouded in garua (although not so during the exceptional 2015-2017 drought, see comments under population assessment). Here, thalli are best developed on dead Cinchona trees, defoliated by chemical control. The lichen is much less exuberant on live trees that still bear a leafy canopy. It is generally absent from closed canopy of Miconia robinsoniana, an endemic shrub that forms the dominant, characteristic vegetation at this altitude. Only where the canopy of this shrub has not yet closed due to disturbance, the lichen can rarely be found (e.g., one site on San Cristóbal). Acantholichen also does not occur where bracken (Pteridium hybrids) dominates the landscape (possibly as a result of anthropogenic fire), particularly on Santa Cruz.
Among the natural Galapagos vegetation, populations of the endemic Acantholichen are now extremely rare. In Santiago, the lichen has only been found (both historic and recent specimens) on liverworts growing on Psychotria rufipes, an endemic shrub listed as Vulnerable [VU B1a,b(iii,v); B2a,b(iii,v)]. On Volcán Alcedo (Isabela) Acantholichen also grows on liverworts on exposed, stunted Zanthoxylum trees, a species native to the archipelago; these thorny snags in the humid, exposed highlands along the crater rim of Alcedo are today the only remains of natural vegetation left from grazing by goats (in the past five year recovery of this vegetation has started, following removal of goats, but competition from introduced plants appears problematic for this recovery).
Similar habitat occurs on Volcán Cerro Azul, the volcano that receives the highest rainfall in the archipelago (its southern flanks are regularly drenched by rising moist sea air). Here, Acantholichen can no longer be found in the now extensive secondary grasslands created by feral cattle and pigs. On Cerro Azul the lichen is therefore restricted to a small remnant population on the tree fern Cyathea weatherbyana [EN A2a,c,e], inside the parasitic crater Cerro Verde, whose steep flanks are inaccessible to grazing (and where populations are therefore presumably stable).
All other known populations are on introduced trees and shrubs, most notably Cinchona pubescens, in the Santa Cruz highlands.
In Santa Cruz, Acantholichen grows on Campylopus on the open ground, where shrubs and ferns cannot establish because of the extremely thin soils, but occasionally also where vegetation has been cleared along paths. These populations are, however, rare. The sites where the lichen grows on this terricolous liverwort are all in close proximity of the exceptionally exuberant populations established on Cinchona. Although sexual reproduction of the basidiolichen remains unknown, it is conceivable that here propagules “rain down” from the trees.
The natural vegetation of the humid Galapagos highlands has significantly been altered. On islands inhabited by humans (San Cristóbal, Santa Cruz, Southern Isabela, Floreana) drastic changes of the landscape are a direct result of agricultural use throughout the fertile highlands. Historic and present day land-use includes clearance of vegetation by fire, cutting and grazing, and the planting of alien species for human consumption. These practices have significantly changed the species composition and structure of natural vegetation types; even sites that were historically not directly used for cultivation and today often “appear” natural, like Miconia scrub around El Puntudo and Cerro Crocker. These have in the past suffered from human intervention (fire, grazing, introduction of Cinchona pubescens and other non-native plants).
Even on islands that are today uninhabited or where in the past human settlements were sporadic, the introduction of invasive species has still had a drastic impact on the humid highland vegetation. Whalers and pirates originally much reduced the only large grazing animal native to all islands: the Galapagos tortoise. Today many populations of these animals have recovered, though mostly not to historic levels. How these tortoises affected the natural vegetation at their original densities is therefore difficult to assess. It is obvious though that introduced alien ungulates (goats, cattle, pigs, donkeys), all had a devastating effect on the natural vegetation throughout the islands.
As a result of human intervention, the natural habitats have thus drastically changed. Particularly for epiphytes, their natural habitat of trees and shrubs will have disappeared, or at least become increasingly rare. Fortunately, most lichen species appear relatively unspecific towards their substrate. Species adapted to open, exposed habitats may initially even have benefited from a more open, moderately disturbed landscape. This may originally have been the case for Acantholichen. In dense Miconia scrub the species was likely never particularly abundant, apart from the edges and fringes of this vegetation type. The native Frullania-Zanthoxylum forests (“brown zone”) were formerly probably quite dense, and since only the most humid areas of this forests will have been suitable for Acantholichen, its habitat was likely quite limited. Some endemic species (Psychotria, Cyathea) presumed to represent typical native habitat of Acantholichen are today threatened. However, the lichen, at least on Santa Cruz, apparently quite successfully switched to alternative habitats, such as Cinchona; these populations are the most exuberant ones known today. Management to control populations of this invasive tree could have a direct, drastic detrimental impact on these important refugia populations, so management must be carefully balanced (see conservation actions).
Whereas it seems that the natural populations of the endemic Acantholichen have declined, it can also be assumed that populations on introduced Cinchona are at least stable or even thriving. With the exceptional 2015-2017 drought this assessment may, however, have to be revised. This highlights the importance of management for this species.
Natural populations of the lichen depend on recovery of the natural vegetation. Habitat represented by species like Cyathea or Psychotria seems particularly important, possibly also the most humid, open areas of Frullania-Zanthoxylum forests. Recovery of the native species in these vegetation types would presumably also result also in a recovery of Acantholichen populations. Succession processes on the islands where goats have been removed should therefore be monitored. For the lichen, the most humid and most exposed habitat sites appear to be most important. Succession patterns and disturbance from rapid growth of invasive plants, in the absence of high population densities of tortoises, may result in very dense, closed vegetation. This could directly impact the last remaining, small native populations of Acantholichen.
Particularly important therefore is the refugium population of Acantholichen on Cinchona pubescens in Miconia scrub near El Puntudo/Cerro Crocker on Santa Cruz Island. The best developed thalli of Acantholichen are found on the dead stumps left standing from chemical control of Cinchona. The current practice of population reduction by chemical control of Cinchona, without mechanical removal of dead trees, appears to be an almost ideal management option. This control of Cinchona nevertheless needs to be carefully evaluated. It is not known, for example, how long dead trees carpeted in Frullania remain standing and will thus be available for Acantholichen colonization. Also, turn-over rates, i.e., generation times, how long individual lichen thalli live, are completely unknown. Sexual reproduction of the lichen has not yet been documented; it is possible that the species exclusively reproduces by asexual propagules (most likely thallus fragments).
Regular and frequent Cinchona control (e.g., the attempt to eliminate most seedlings) may prevent sufficient re-establishment of new adult trees as necessary prerequisite for producing more dead stumps. Even if complete Cinchona eradication is prohibitively expensive, the National Park may eventually attempt to restore natural highland vegetation by cultivating closed Miconia canopy without Cinchona trees, and particularly without new adult trees establishing again. This might be considered a more “natural” landscape than scattered dead or even live trees, but a management strategy that focuses on species diversity, rather than on an “ideal” landscape must find a compromise. This might not be difficult, because Acantholichen is not common wherever Cinchona occurs. On the contrary, it appears restricted to a few sites. In these pockets a balanced approach that permits establishment of few Cinchona trees may be the most appropriate management option.
Conservation of the species relies on monitoring natural vegetation recovery and implementing a management plan of Cinchona control that leaves sufficient trees standing for their Acantholichen populations. Both conservation actions should be outlined in a species action plan and area-based management plan for the few known locations of this species.
Presently, all assumptions about population size, distribution and trends of A. galapagoensis, particularly at native habitat sites but also on Cinchona pubescens, are based on a ten year species inventory of Galapagos lichens (2005-2015). This archipelago-wide inventory yielded the preliminary evidence presented here. The inventory was not focused specifically on Acantholichen galapagoensis, and a more thorough survey of similar habitat may yield additional localities where other populations of this species may still be found, yet it is doubtful if a few additional localities would drastically change the assessment presented here.
Research into the ecology of the species is more urgent. Though the species is endemic to Galapagos and clearly distinct from A. pannarioides (Dal-Forno et al. 2015), the life-history of this endemic basidiolichen remains poorly known (sexual reproduction is unknown, propagules are most likely thallus fragments). It is therefore not known, for example, how much genetic diversity is present in its different populations. It is possible, for example, that the extremely exuberant specimens on Cinchona (or even on the footpath below) is part of a single, clonal population. If this is the case, the conservation status of the species would need to be considered even more dire than presently assessed. Although clonal organisms are often widely distributed and abundant, this is clearly not the case here. Populations of Acantholichen galapagoensis, even if reproducing only asexually, are clearly much restricted.
Also: how climate change may affect the populations is currently unknown. During 2015-2017 the archipelago was hit by an extreme, unusual drought and refugia populations particularly on Santa Cruz should be monitored whether they will recover, when it becomes more humid again.
Dal-Forno, M., Bungartz, F., Yánez-Ayabaca, A., Lücking, R. & Lawrey, J.D. (2017) High levels of endemism among Galapagos basidiolichens. Fungal Diversity, DOI10.1007/s13225-017-0380-6.
Dal-Forno, M., Lücking, R., Bungartz, F., Yánez-Ayabaca, A., Marcelli, M.P., Spielmann, A.A., Coca, L.F., Chaves, J.L., Aptroot, A., Sipman, H.J.M., Sikaroodi, M., Gillevet, P. & Lawrey, J.D. (2016) From one to six: Unrecognized species diversity in the genus Acantholichen (lichenized Basidiomycota: Hygrophoraceae). Mycologia 108(1): 38-55.
Jørgensen, P.M. (1998) Acantholichen pannarioides, a new basidiolichen from South America. The Bryologist 101(3): 444-447.
Lawrey, J.D., Lücking, R., Sipman, H.J.M., Chaves, J.L., Redhead, S.A., Bungartz, F., Sikaroodi, M. & Gillevet, P.M. (2009) High concentration of basidiolichens in a single family of agaricoid mushrooms (Basidiomycota: Agaricales: Hygrophoraceae). Mycological Research 113: 114-1171.
Lücking, R., Lawrey, J.D., Sikaroodi, M., Gillevet, P.M., Chaves, J.L., Sipman, H.J.M. & Bungartz, F. (2009) Do lichens domesticate photobionts like farmers domesticate crops? Evidence from a previously unrecognized lineage of filamentous cyanobacteria. American Journal of Botany 96(8): 1409-1418.
Yánez-Ayabaca, A., Dal-Forno, M., Bungartz, F., Lücking, R. (2012) A first assessment of Galapagos basidiolichens. Fungal Diversity 52:225-244.