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9ESTABLISHING NEW WORLDSTHE LICHENS OF PETERSHAMAnne Pringle

Lichens Are Ancient WorldsWhat was once thought to be a mutualism involving two species may

be an entangled symbiosis of thousands of species, interacting in

every conceivable fashion. A lichen is not just a fungus and its photo-

synthetic algae. Lichens house hundreds, thousands, or perhaps tens

of thousands of other species within the thallus, including other kinds

of fungi and myriad bacteria. Bacterial diversity peaks at the center of

a thallus, while the various edges house relatively fewer taxa.1 Bacterial

communities at the centers of different lichens resemble each other,

while edges house more random assemblages. Even something as basic

as reproduction may involve bacterial communities. Lichens often

reproduce asexually, and within asexual propagules, the lichen pack-

ages its bacteria.2 Perhaps the countless additional bacteria and fungi

associated with a thallus provide benefits to the lichen, or perhaps

many are antagonists. While we are far from a perfect understanding

of the natural history within a lichen, it is clear that lichens are worlds

unto themselves.

Moreover, these worlds have existed for a very long time. The ear-

liest known fossil lichen dates to the Early Devonian. Chlorolicheno-

mycites devonicus was discovered in rock 415 million years old from

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the Welsh Borderland.3 This species, along with other lichen species,

species of nonlichenized fungi, and free-living algae and cyanobacteria,

may have formed extensive, diverse communities across large swaths

of Early Devonian landscapes. These landscapes would have looked

almost unlike anything we know today. At a time before modern plants

evolved, these communities would have seemed like living, textured,

and tufted carpets, and perhaps in some places one would have also

seen the gigantic, three-meter-tall Prototaxites, an enigmatic life-form

sometimes interpreted as the sporocarp of an enormous fungus.

I study a complex of lichens within the genus Xanthoparmelia. The

taxonomy of the genus is controversial, and one paper uses Xantho-

parmelia to argue against morphology as an appropriate descriptor of

species boundaries.4 To avoid the debate, I will simply use the generic

name Xanthoparmelia. I work with populations growing on tomb-

stones of the North Cemetery in Petersham, Massachusetts (Figure

G9.1). Because I am curious about the natural histories of groups of

lichens growing on different tombstones, I go to the cemetery each

year and track the status of approximately eight hundred individuals.

Figure G9.1. The North Cemetery of Petersham, Massachusetts. Tomb-stones are novel habitats for lichens. Photograph by Anne Pringle.

Establishing New Worlds ● G159

Landscapes Are ChangedNew England Xanthoparmelia grow on rocks, or structures made from

rock; in Petersham the lichens are commonly found on stone walls as

well as in cemeteries. Before European settlement, the lichens would

have grown on rocks or boulders within forest clearings or at forest

edges. Exposed boulders are a regular feature of primary forests but

are not abundant (Figure G9.2).

When Europeans settled in Petersham, coming west from Boston

and east from the Connecticut River Valley, forests were cleared to

make way for farms. Most land was cleared for pasture, but around

North Cemetery, up to 15 percent of the land was used for agriculture.5

Agriculture requires workable soil, and to farm a field, a farmer must

first dig the rocks out of the ground. These rocks were often used to

build massive stone walls (Figure G9.3; note both Figure G9.2 and Fig-

ure G9.3 offer a view from the same vantage point).

In Petersham, farmers built 436 miles of rock walls. Whereas walls

were built to suit the individual farmer, New England cemeteries

were built according to very specific town plans;6 often, in addition to

a central (or center) cemetery, four cemeteries were built away from

the town center in each of the cardinal directions (north, south, east,

and west). Thus, the North Cemetery of Petersham is approximately

three miles north of Petersham’s Center Cemetery. Whereas there are

hundreds of tombstones within the Center Cemetery, the North Cem-

etery houses only a few dozen.

The lichens followed the rocks. New England tombstones are

often covered with a profusion of lush lichen growth, and lichens are

a nearly universal feature of old stone walls. If the habitats of Xantho-

parmelia were relatively rare before European settlement, by 1850,

they were not, and although there are no data that track the rise of

lichen populations, today a sunny meter of stone wall easily houses

several hundred Xanthoparmelia. When Petersham was a town of 436

miles of exposed stone walls, it’s quite likely there were hundreds of

thousands of Xantho parmelia on the walls.

New England agriculture peaked in the early nineteenth century.

After about 1850, the Louisiana Purchase, California Gold Rush, and

industrialization of cities including Holyoke opened up new opportu-

nities for Petersham farmers.7 The Erie Canal and railroads made it

possible for midwestern farms to move farm goods east, making local

Figure G9.3. A diorama of forest clearing and agriculture, circa 1830 C.E., on display at the Fisher Museum of Harvard Forest. Note the extensive stone walls around fields and along roads; lichens would have quickly established on these new habitats. In Petersham, approximately 436 miles of stone walls remain, but often walls are found within regenerated forest. Photograph by John Green, Harvard Forest, Harvard University.

Figure G9.2. A diorama of pre-European settlement forest, circa 1700 C.E., on display at the Fisher Museum of Harvard Forest. Note the rock outcrop at bottom left; these kinds of surfaces are the original habitat of Xanthoparme-lia lichens. Photograph by John Green, Harvard Forest, Harvard University.

Establishing New Worlds ● G161

farming less profitable. Agricultural lands were abandoned, and for-

ests grew up around the stone walls. Although some cemeteries were

also abandoned, for example, Petersham’s Poor Farm Burial Plot,

many remain in continuous use, for example, both North and Center

Cemeteries. Probably many lichens died as stone walls and abandoned

cemeteries were shaded—Xanthoparmelia need light to grow. But once

again, there are no data to suggest exactly how populations changed

during and after farm abandonment.

Worlds Are MovedAs the lichens dispersed to the tombstones and walls, they would have

carried their bacteria with them. One class of bacteria found in Xantho-

parmelia is the Alphaproteobacteria. The class is enormously diverse,

but its species often grow in symbiosis, for example, as plant mutualists

capable of fixing nitrogen from air into metabolically useful compounds

or as insect parasites capable of turning insect males into females. The

class was the source of mitochondria and plant chloroplasts, and the

origin of eukaryotes is intimately associated with Alphaproteobacteria.

In this class, horizontal gene transfer, or the movement of genes across

species boundaries, is rampant, and one species is used to facilitate the

movement of foreign DNA into plant genomes. Although we have a

poor understanding of what the Alphaproteobacteria do within Xantho-

parmelia (and it is unlikely the Xanthoparmelia house insect parasites!),

we do know the lichens enabled the movement of entire, complex com-

munities across the New England landscape.

ImmortalityHow long does each world last? I started to work with lichens because

I am fascinated by an idea that filamentous fungi are immortal. Aging,

or senescence, is defined as a decreased probability of reproduction,

and increased probability of death, with time. An immortal organism

never ages, and the probabilities of reproduction or death may take

unusual patterns. An immortal organism can still be killed, for exam-

ple, it can be run over by a bus or chopped to bits with an ax, but it is

no more likely to die of natural causes at age x + 1 than it was at age

x. Human aging is an intuitive concept; an eighteen-year-old is more

likely to have a baby and less likely to die than an eighty-year-old.

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What it means for a fungus to age may be less intuitive. Remember

that the fungus forming the foundation of any lichen thallus grows

as a network. It’s a filamentous fungus. In contrast, yeasts, like the

yeasts you use to bake bread or brew beer, are unicellular fungi. Each

cell eventually stops budding and dies. Yeasts are not immortal. But

it’s not clear if filamentous fungi stop reproducing, or are more likely

to die, as they grow older. Moreover, because there are hundreds of

thousands of species of filamentous fungi, it’s not clear whether or

how data from one species would translate across the kingdom.

To date, research on aging within the filamentous fungi has focused

on the dung fungus Podospora anserina. This fungus grows only on

animal poop, and these habitats are ephemeral; dung quickly decays.

Because its habitats constantly appear and disappear, P. anserina

hasn’t had a chance to maintain or evolve immortality. In fact, if you

grow it in a petri dish, you will find that it ages. The dynamics shaping

the evolution of aging in P. anserina are not completely understood,

but perhaps the species has lost the ability to repair DNA damaged

by the normal wear and tear of daily growth. Because it doesn’t last to

old age in nature, there would be no reason to maintain repair mech-

anisms. In fact, most fungi from ephemeral habitats appear to age.8

But boulders and rock walls last a very long time. Have the filamen-

tous fungi that form the basis of the Xanthoparmelia escaped senes-

cence? To understand that question, I decided a long time ago that I

needed to understand the dynamics of natural populations. I wanted

demographic data: data describing the births, growths, and deaths of

many individuals. Aggregate data would enable me to calculate the

probabilities of reproduction and death over time and understand if

demographic patterns are typical, for example, if they look like human

demographic patterns, or if patterns are somehow different from the

patterns of animal or plant species.

MethodsWhen I go to the cemetery, I focus on a subset of tombstones. I have

permission from both the Petersham Cemetery Commission and

families to trace and photograph the lichens, although nothing I do

causes any damage to either the tombstones or the lichens. Many of

the tombstones belong to past directors of the Harvard Forest, includ-

ing Ernie Gould and Hugh Raup (Figures G9.4 and G9.5).

Figure G9.4. The Gould tombstone. Xanthoparmelia are green, but black and gray lichens also grow on the tombstone. Photograph by Anne Pringle.

Figure G9.5. Hugh Raup (right, standing) and Ernie Gould (left, seated) teaching at the Harvard Forest, 1965. Harvard Forest, Harvard University.

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Because Gould and Raup were foresters, concerned with ongoing

changes to local landscapes, I like to think they wouldn’t mind hav-

ing research done on their tombstones; in fact, I like to think they’d

find it hilarious.9 I know I would. Each fall, I draw maps of the lichen

populations. I place transparent, plastic sheets over the various tomb-

stone surfaces and carefully trace the perimeter of target individuals

(Figure G9.6).

The letters and numbers carved into the rock enable accurate ori-

entation of the previous year’s maps at each new census, and I can

easily identify every individual every year. I started the survey in

2005. At first, I would trace entire populations, but after a few years,

this was too much, and I stopped recording new births. Changes in

Figure G9.6. Every year, I trace maps of the Xanthoparmelia lichens growing on a set of tombstones. From year to year, I measure growth, reproduction, and death. Photograph by Anne Pringle.

Establishing New Worlds ● G165

individual perimeters from year to year provide growth rate data,

but I also note every individual’s reproductive status and health and

occasionally collect data from various subsets of individuals to answer

other questions.

The Persistence of Dispersed WorldsPatterns of reproduction and death among the Xanthoparmelia are

very different from patterns described for many animals, and often

different from patterns described for plants. As an individual lichen

grows older, it grows larger, and as the lichen grows larger, it repro-

duces more. The Petersham Xanthoparmelia are largely asexual, and

as an individual grows larger, more surface area is available for the

construction of asexual propagules. Lichens occasionally fragment,

but in this cemetery, it doesn’t happen very often, perhaps because

disturbance is rare. While I’ve recorded the disappearance of small

lichens, which may wash off the rock in bad weather or be overgrown

by larger neighbors, I’ve yet to record the death of a large lichen. As

lichens grow older, the probability of death seems to decrease.

But as the years in the cemetery passed, I began to wonder about

how I was describing death, really because of the data of a few indi-

vidual lichens. I recorded death when an entire thallus disappeared.

Lichens grow at their edges, and if there are no barriers to growth,

a thallus will expand in a more or less circular fashion. Centers are

older than edges, and by now, I can date with some exactness the age

of particular tissues.10 Remember that bacterial communities at older

centers are different from bacterial communities at younger edges.

Perhaps succession is at work within this world, in the same way that

abandoned New England farms start as grasslands but eventually

become forests. Time influences landscapes, and as a lichen grows

older, perhaps bacterial communities harmful to the foundation fun-

gus form at the center. In response, the fungus may kill its center, and

sometimes I do see large lichens with missing centers. In fact, this is

the classic definition of death in lichenology: if the center falls out, the

lichen is dying. I’m still not sure that’s true—won’t the edges grow on

forever? But I wonder if aging is a feature of parts, or modules, of an

individual thallus, even if it isn’t a feature of the thallus itself.

Petersham is beautiful, and it’s easy to go for long walks in the sur-

rounding forests, but Petersham is a human habitat, and there isn’t

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one square inch that hasn’t been influenced by people. Trails often

cross abandoned stone walls. Lichens on old stone walls are a quin-

tessential feature of the landscape, signals of clean air and stability.

New stone walls don’t have lichens, and neither do walls in polluted

environments, but the lichens and sometimes mosses of Petersham’s

stone walls can form an almost continuous carpet of green.

These lichens are nature. The word nature is complicated, I know,

but if in its simplest sense nature means something alive, and not built

by humans, then lichens are nature, even if they grow in altered land-

scapes. We built Petersham and, by doing so, built the lichens substrates

on which to multiply, but they came on their own. Entire worlds estab-

lished, and the worlds aren’t static. While the interactions within each

extant Xanthoparmelia may play out almost imperceptibly, they will

influence the growth of the species within, creating a dynamic interior

ecology. And whether it is the interactions or something else shaping

the evolution of aging, it’s clear these dynamic worlds will persist for a

very long time.

ANNE PRINGLE works with species whose life histories and body plans seem very different from our own. She explores the fungi: their asso-

ciations as lichens and with plants, their ecological roles in a changing

world, and the nature of their individuality. She is associate professor

of botany and bacteriology at the University of Wisconsin, Madison.

Notes 1. A. A. Mushegian, C. N. Peterson, C. C. M. Baker, and A. Pringle, “Bac-

terial Diversity across Individual Lichens,” Applied and Environmental

Microbiology 77 (2011): 4249–52.

 2. I. A. Aschenbrenner, M. Cardinale, G. Berg, and M. Grube, “Microbial Cargo: Do Bacteria on Symbiotic Propagules Reinforce the Microbiome

of Lichens?,” Environmental Microbiology 16 (2014): 3743–52.

 3. R. Honegger, D. E. Edwards, and L. Axe, “The Earliest Records of Inter-nally Stratified Cyanobacterial and Algal Lichens from the Lower Devo-

nian of the Welsh Borderland,” New Phytologist 197 (2012): 264–75.

 4. H. T. Lumbsch and S. D. Leavitt, “Goodbye Morphology? A Paradigm Shift in the Delimitation of Species in Lichenized Fungi,” Fungal Diver-

sity 50 (2011): 59–72.

 5. D. R. Foster and J. D. Aber, ed., Forests in Time: The Environmental Con-

Establishing New Worlds ● G167

sequences of 1,000 Years of Change in New England (New Haven, Conn.:

Yale University Press, 2004).

 6. D. R. Foster, pers. comm., November 2015. 7. Ibid. 8. T. D. Geydan, A. J. M. Debets, G. J. M. Verkley, and A. D. van Diepenin-

gen, “Correlated Evolution of Senescence and Ephemeral Substrate

Use in the Sordariomycetes,” Molecular Ecology 21 (2012): 2816–28.

 9. H. M. Raup, “The View from John Sanderson’s Farm: A Perspective for the Use of the Land,” Forest History 10 (1966): 2–11.

10. Mushegian et al., “Bacterial Diversity across Individual Lichens.”