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Latent Extinction—The Living Dead

Abstract and Figures

Trees and many other organisms that dot the tropical agroscape are often living dead. These are those individuals that have been stripped of the ecological circumstances that allowed them to be a reproductive member of their populations but are living out a physiological life. The term may also be applied to a portion of a population or a patch of vegetation. There are degrees of “living deadness.” A living dead individual or even population may be resuscitated through ecosystem restoration. Ecosystem alteration by humans frequently produces living dead, but living dead are also part of natural ecosystem structure. The term and concept are conveniently applied to individuals that live long enough or are conspicuous enough to be included in the lay perception of the environment. The living dead are, in their sum, a latent extinction of a species in a place. This renders them a perceptual problem in the psychology of tropical conservation because their presence obfuscates pending extinction. But living dead are also primary elements of natural processes of local extinction, immigration, and population-community structural dynamics in response to short- and long-term environmental change, be it natural or anthropogenic. Extra-tropical habitats and extreme tropical ecosystems may have fewer living dead than do complex tropical ecosystems, but they are nevertheless present. As magnificent as the living dead may be on the tropical countryside, I suggest that we not be distracted by attempting to save them, but rather that we focus our conservation efforts on saving large blocks of wildland ecosystems that are relatively complete and (it is hoped) relatively poor in living dead.
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Latent Extinction
F
The Living Dead
Daniel H Janzen, University of Pennsylvania, Philadelphia, PA, USA
r2001 Elsevier Inc. All rights reserved.
This article is reproduced from the previous edition, volume 3, pp
689–699, r2001, Elsevier Inc.
Glossary
Agroscape The agricultural, ranching, and plantation
countryside, with its roads, irrigation ditches, buildings, and
so on. The agroscape stands in contrast to the wildland
countryside that is not directly managed by humanity (though
it is strongly impacted by it). The agroscape intergrades with
wildlands in the form of woodlots, abandoned fields, poor
soil sites, hedgerows, and edges of wildlands.
Living dead An individual stripped of the ecological
circumstances that allow it to be a reproductive member of
its population, but which is living out its physiological life.
Living dead are most easily observed as large trees
remaining on the agroscape, but they are also present in
natural ecosystems.
Megafauna Large mammals that are wolf-sized,
deer-sized, and larger. Commonly used in reference
to the many species of extinct ‘‘Pleistocene megafauna’’ that
9000 years ago populated the New World. The elimination
of this megafauna by hunting (of the herbivores) and
starvation (of the herbivore deprived carnivores) was
probably the first, and certainly the most dramatically
irreversible, of the anthropogenic macroalterations of New
World ecosystems. Today, of the extinct Pleistocene
megafauna, only the horse remainsFevolutionarily
invented in the New World but surviving in the Old World
until brought back as a gift from the Pleistocene by Spanish
soldiers.
Introduction
The idea of the living dead has gradually emerged in my eco-
logical understanding as I have lived past and around the ma-
jestic forest giants left standing as the agroscape creeps into Costa
Rica’s forest ecosystems over the past 4 decades (Figure 1 and
Janzen, 1986a, 1986b). This creep gradually converts the forest
to an agroscape of pastures, fields, and roadsides dotted with the
occasional adult tree but few or no juveniles. This is an agroscape
where a magnificent flower crop now stands bee-less, an agros-
cape where fruit crops lie rotting below the pasture tree, an
agroscape where tree seedlings wither in the dry-season sun or
are turned to smoke in the dry-season anthropogenic fires.
I begin this article with a focus on adult large trees and use
familiar examples from the Costa Rican countryside. To create
breadth, I suggest that you join these verbs with the nouns
from the ecosystems you know. This is a conservation biology
question, but it applies to more than that, and it applies across
the once-forested tropics as well as elsewhere.
Looking across the tropical landscape, the eye is greeted by
stately single trees (Figure 2), by patches of forest, by the blaze
of a colorful flowering episode. Put an inventory to the plant
species in a field, in a valley, in an ecosystem. All these species
appear in the list. All is more or less well, we conclude, as
96.4% of the species that were here 50 years ago are still
present. But are they? How many of them are living dead, part
and parcel of latent extinctions?
We live a perceptual lie as we bustle about our agroscapes.
That single stately green Dipteryx or Hymenaea or Swietenia or
Enterolobium, standing in a field, pasture, or roadside, is often
just as dead as if it were a log in the litter or the back of a
logging truck. That tree was birthed in some favorable cir-
cumstance, a circumstance for pollination, seed dispersal, seed
germination, and sapling survival.
But one or more of these circumstances is now gone. It was
carried away with the forest, put on the hunter’s table, pesti-
cided out of existence, or global warmed into oblivion. The
long-lived tough adult lives out its physiological life, in the
absence of the carpenter with a chain saw, but it is evo-
lutionarily dead. Its pollen no longer flows to other members
of the population, its seeds are no longer carried away from
seed predators, or its seeds are no longer carried to a favorable
site for seedling growth and sapling survival to adulthood.
But because the adult lives on, we are lulled into thinking
that the environmental damage really is not all that bad, that
extinction has not already occurred. If we can still show the
tree to our children, it seems not to be extinct. It is so big and
green and strong. Every year we see its flowers, and maybe we
even see its fruits on the ground below. And after all, it has
clearly weathered all that we have thrown at it. What ever can
the matter be?
Humanity’s interaction with the world’s ecosystems has an
enormous perceptual element. We act on what we perceive, be
it threat or opportunity. Much of our conservation pragmatics
and understanding is based on our knowledge that we really
are losing species, losing ecosystems, losing the capacity of the
environment to absorb our footprints. But that knowledge
comes from what we see and measure. If all members of a tree
species were to have the trait that each abruptly falls over dead
the moment that it ceases to be a reproductive member of its
population in its ecosystem, there would be far stronger alarm
cries across the tropics about extinction rates and realities.
If trees, the largest organisms on most of our landscapes, were
very short lived as compared with humans, there would be less
of a perceptual problemFthough just as large a conservation
problem.
When the terrestrial world was covered with forest eco-
systems, the single tree left standing in an aboriginal cornfield
Encyclopedia of Biodiversity, Volume 4 http://dx.doi.org/10.1016/B978-0-12-384719-5.00085-X590
may well have been living dead, but the population from
which it was derived was not usually at risk of anthropogenic
extinction, unless perhaps dependent on a seed disperser tar-
geted by that aboriginal population (Janzen and Martin,
1982). But when the agroscape is dotted with living dead in
the wake of contemporary omnipresent ecosystem alteration,
latent extinction is very real. A tree species may be ranked as
‘‘common’’Fmeaning visible from a car window along many
roadsFyet be effectively extinct in a county, state, or region.
And since the agroscape now stretches from horizon to hori-
zon, the plant may well be absolutely extinct, since all of its
former range may be populated by living dead.
Deforestation and the Living Dead
The forest need not be removed to convert trees to living dead.
It is just that when the forest is partly removed, there is a very
high chance that this alone will ecologically deprive many
individuals of the remaining tree species sufficiently to convert
them to living dead status. And, it certainly leaves the living
dead very visible.
But even when the forest is left in place, that is no guar-
antee of a healthy tree population. When the Pleistocene
hunters and their carnivorous helpers hunted out the neo-
tropical mastodons and gomphotheres, the glyptodonts and
camels, the ground sloths (Janzen, 1983b; Janzen and Martin,
1982), they did not do it by forest clearing. For decades to
millennia after this 9000-year-old event, many of the remnant
individuals of the tree populations that these big mammals
dispersed (Figure 3), and for which they created safe sites for
seedlings by their browsing and trampling, would have been
living dead scattered in the forest.
If some particular speciesFa pollinator or dispersal agent,
for exampleFin the forest is extinguished, by whatever cause,
there will often be surrogates and alternates that will assume,
in some form, some portion of the ‘‘role’’ of the extinguished
mutualist. The tree species will live on, albeit in some other
ecological morph, and therefore in some technical sense will
not be extinct. The tree that was ‘‘dependent’’ on the
Figure 1 Living dead trees isolated in pasture at the edge of the agroscape (background) as it creeps into old growth forest (foreground). Los
Naranjos, Sector Cacao, Area de Conservacio
´n Guanacaste, July 29, 1987.
Figure 2 A living dead Terminalia tree stands in silhouette, left
behind as the rain forest was cleared around it, the natural tree falls
in which its seedlings might have survived long since removed.
Rincon Rainforest, Area de Conservacio
´n Guanacaste, January 6,
2000.
Latent Extinction
F
The Living Dead 591
extinguished species will not, then, be living dead. But the
devil is in the details. We need to go case by case. The suite of
interactants with a tree species generates a given seed shadow,
pollen rain, sapling demography, and microgeographic dis-
tribution. Remove one species of interactant. The entire
n-dimensional hyperspace shifts in this or that direction. In
some places this is toward eventual extinction, in other places
it is just a change in demography and microgeographic
distribution.
The history of any surviving species is that it must have
survived thousands of such handoffs from one mutualist to
another, from one moment to the next (e.g., Hallwachs,
1986). What bumps individuals into the category of living
dead is the serendipitous event of losing irreplaceable part-
ners. Humanity has a way of removing not only partners, but
whole suites of them, as well as altering the physical en-
vironment. Our thoroughness and omnipresence creates eco-
logical irreplaceability. Yes, when we lose one ground sloth, a
glyptodont picks up some of the slack, though the tree is now
a different beast. And at some time, likely as not, some new
slothoid arrives by evolution or immigration over the mil-
lennia. But lose all these big mammals at once, and the result
is guaranteed to be large arrays of living dead.
We have all been nourished by the marvels of evolutionary
understanding, leading to the temptation to wonder if rapid
evolution will not resuscitate a living dead population, if not
many of its individuals. Novel pollinators, dispersal agents,
fruit morphology, flowering phenologyFall could save the
day. In theory yes, but in reality not on the timescales or-
dained by humanity’s charge across the landscape. How long
will it take to evolutionarily reinvent a neotropical herbivor-
ous/frugivorous megafauna? Fracture the remaining forest,
with its living dead, into small ecological islands (also known
as national parks and reserves). Thereby create ideal circum-
stances for rapid and novel evolution. We still cannot expect
natural selection to create a mastodon from a white-tailed deer
in anything like the speed required to be an antidote for
neotropical rain forest anthropogenic alteration, beginning
with the megafauna extinctions.
Certain kinds of habitat destruction are compatible with
some tree natural histories. Two common trees, the guanacaste
(Enterolobium cyclocarpum, Fabaceae) and jicaro (Crescentia
alata, Bignoniaceae), owe their contemporary prominence on
the Mesoamerican Pacific coastal landscape to a particular
kind of habitat destruction. For both, large mammalsFsuch
as free-ranging horsesFswallow the seeds while eating the
content of indehiscent fruits fallen below the parent tree
(Figures 3 and 4), and later defecate them in open sunny
habitats (Janzen, 1981, 1982a, 1982b). Forest clearing unto
brushy pastures and scraggly roadsides, populated by widely
circulating working horses, maintains a healthy population of
reproducing guanacaste and jicaro trees in a precarious bal-
ance with humanity.
What did these trees do before the Spaniards brought the
horse back from its Old World refuge after its neotropical
extinction by Pleistocene hunters (Janzen and Martin, 1983)?
They probably survived in a peculiar habitat characterized by
ample insolated ground yet sufficient rain for there to be large
trees and sloppy seed predator rodents (or human fruit and
seed harvesters), which offered sufficient seed dispersal. River
edges, marsh edges, and the interface between tropical dry
forest and desert are such habitats, and the aboriginal village/
field edge adds a serendipitous fourth. The Spanish working
horse (Figure 4) found the fruits abandoned by their extin-
guished ancestors and spread these two trees so thoroughly
that today they are viewed by Mesoamerican societies as native
and natural. And, in the case of Enterolobium cyclocarpum, cattle
are surrogate horses (Janzen, 1982a).
However, as the motorbike and car replace the horse today,
and as the cattle industry fades, these two trees are left as very
visible living dead scattered across the former ranch lands,
their abundant fruits rotting below the parent tree, the newly
Figure 3 A living dead Crescentia alata fruit crop presented to earthbound extinct megafauna (Figure 4). Sector Poco Sol, Area de Conservacio
´n
Guanacaste, May 28, 1988.
592 Latent Extinction
F
The Living Dead
germinated seedlings killed by fungal pathogens nourished by
the annually replenished seed crop, and the rare escaped
seedling killed by herbicides, grass fires, and cosmetic
cleansing.
When is a Tree not Living Dead?
Earlier I noted that if each member of a tree species were to
abruptly fall over dead the moment that it ceases to be a re-
productive member of its population in its ecosystem, there
would be far stronger alarm cries across the tropics about
extinction rates and realities.
However, the isolated tree, left an adult in the open as the
forest is mined away from around it (Figure 2), is not neces-
sarily or automatically a member of the living dead, or at least
not necessarily at that moment. At least two circumstances
may help to avoid this label. First, the pollinator community
and the seed dispersal community for that tree may still be
of a structure such that they confer sufficient amounts
and patterns of their services and do so with the new repro-
ductive phenology that will be expressed by the tree in its
‘‘new’’ habitat. And males do have fitness. A plant may never
set a fruit or never have a surviving seedling from its
seed crop, yet it still may be very much a member of the
reproducing population (e.g., Aldrich and Hamrick, 1998).
Plants contribute pollen ‘‘outward’’ as well as receive it from
unseen members of the population. There may be some
circumstances where this or that member of the pollinator
guild will in fact carry pollen from that isolated tree back
into the forest. At least potentially this may remove the living
dead label.
Second, the new pattern of seed/seedling/sapling safe sites
for that species may be sufficient for population survival, even
if different. A novel demography, reproductive phenology, and
microgeographic structure will ecologically emerge, reflecting
the serendipitous matching of the tree’s traits to these new
conditions.
For the survivor, such ecological fitting (Janzen, 1985)of
an individual (or a population) into the environment newly
thrust upon it is the same process as occurs when a tree species
is anthropogenically introduced to a new place. Whether
introduced by humans or by natural processes, its survival
there demonstrates that it has ecologically fit in. Such intro-
duction may occur into a natural ecosystem or one variously
anthropogenically perturbed. Sloppy deforestation may create
many living dead, only mildly impact some other species, and
favor yet new introductions into the region by having removed
competitors or consumers.
A population of plants in a newly altered landscape is not
necessarily at a given moment either ‘‘dead’’ or ‘‘alive.’’ Just as
the relationships of an individual to its ecological circum-
stances may decay slowly, it is also easy to visualize a popu-
lation being sufficiently anthropogenically impacted that it
gradually decays over several decades-to-centuries-long gener-
ations. This state of decay is an intermediate between living
dead and ‘‘normal surviving.’’ The portion of a population of
trees at some geographic point may be in a constant state of
swinging between being ‘‘okay’’ and living dead, as its asso-
ciated climate and community of interactors goes through
their own changes.
A species’ population in its totality may also be waxing or
waning in geographic coverage, density, ‘‘living deadness,’’ or
all three. Living dead are found at the geographic or demo-
graphic margins of all populations. It is just that human ac-
tivity in ecosystem modification (elimination, simplification)
simultaneously impacts so many species, and is so omni-
present, that it creates large numbers of living dead in the
same place at the same time. These then carry the tragic per-
ceptual load of tricking us into thinking that all is much more
well than it actually is.
But ecological neutering, expressed as here in the terms
‘‘living dead’’ or ‘‘latent extinctions,’’ is not restricted to the
circumstance of the single tree in the field or a single portion
of a population. The living dead are an integral part of natural
age-structured mortality. Any field biologist can identify a large
number of young individualsFseeds, seedlings, saplingsF
that have a vanishingly small chance of survival as individuals.
The forest understory is densely populated with them, as is each
squirrel’s winter seed cache, as is the patch of seedlings below
the healthy parent tree, as is the ground covered with ephiphyte
seeds that fell past the branches of the trees above, as is the floor
of the cave littered with bat-dispersed seeds. A very large part of
the world’s herbivore machine is run with this fuel and actually
should be labeled ‘‘detritivore’’ rather than herbivore.
The implications for evolutionary biology are huge, given
that no matter how much herbivory occurs on these living
Figure 4 An earthbound extinct megafauna returned from the Costa
Rican Pleistocene by Spanish immigrants, breaking a Crescentia alata
fruit (Figure 3) to eat the molasses and seeds inside. Sector Santa
Rosa, Area de Conservacio
´n Guanacaste, 1980.
Latent Extinction
F
The Living Dead 593
dead, there can be no natural selection inflicted on the food
populations.
Living dead adult individuals are also a prominent part of
many undisturbed habitats and ecosystems. These are the
waifs, the strays. Each of these is a plant whose seed arrived,
grew to an adult, but found itself in a place lacking whatever is
needed to maintain a viable population (Janzen, 1986c). In
complex interwoven tropical habitats and ecosystems, the
species list in a given place may contain as many as 10 to 20%
of these kinds of living dead. For example, if a valley-bottom
forest is eliminated, over time a significant number of tree
species may disappear from the adjacent ridge, not because of
any direct impact on the ridge forest but because the portions
of the populations that were there are no longer maintained
by seed flow into them from the valley bottom. This phe-
nomenon is particularly visible where a particular soil or slope
is thoroughly cleared for a crop, and the natural vegetation is
left relatively intact in a neighboring habitat, ostensibly to
protect it. Some species disappear because the conserved
habitat did not really have its mutualist animals and physical
climate conserved, or because it is too small, but others dis-
appear simply because they were naturally occurring living
dead.
Not to belabor the obvious, a tree standing dormant in the
tropical dry season is not reproducing in the narrow sense, but
it is also not necessarily living dead. But this is tricky for the
observing human. We are very accustomed to being around
trees that are not, at that moment, undergoing anything that
appears to be reproduction, yet are members in good standing
of quite surviving populations. The living dead tree does not
display anything much different at first glance. Recognition of
living dead status requires in-depth knowledge of its activities
over decades, requires knowing if and where its pollen is
going, and requires knowing where its seeds are moving to
and what happens to them when they get there. This under-
standing is not acquired with the casual glance (e.g., Aldrich
and Hamrick, 1998; Curran et al., 1999; Hallwachs, 1986).
What of Small Plants?
The isolated tree in the pasture has been a convenient illus-
trative example, but the world to which these ideas apply is far
greater than that of large tropical trees. A small herbaceous
plant may be a perennial with longevity like that of a tree.
When the euglossine bees are extinguished through forest
partial clearing, a Catasetum orchid they pollinated is left high
on the main trunk of a shade tree left behind, a living dead in
its own right. The orchid may flower for a century, waiting in
vain for its long-distance pollinators (Janzen, 1974). They are
long gone, their year-round nectar and pollen sources turned
to charcoal. A living dead clump of perennial grass on a
landslide scar may for many decades produce its small
hard seeds, designed millions of years ago for a trip through a
seed-dispersing, now-extinguished, large herbivore to a new
disturbed site (Janzen, 1984). It finally succumbs to its indi-
vidual sterile fate as the landslide scar revegetates to forest.
A living dead herbaceous morning glory (Convolvulaceae),
sprouting and flowering year after year into the insolated
roadside ditch from its underground tuber, may never again
see the bees that once moved among its flowers and the
flowers of the many other forest-edge species that once sus-
tained them (e.g., Frankie et al., 1998).
But as mentioned earlier for a population of trees, even a
population of annuals may also be a living dead population.
Yes, each year it may flower and seed and disperse and then
again germinate with the next rains. But did it make ‘‘enough’’
seeds? Were they set at the ‘‘right’’ time? Did they have the
right genetic composition? Did they move to the right safe
sites? Were those sites there to be moved to? Does the popu-
lation do all this and much more to hold its place in the
naturally shifting nature of its surroundings? Each year the
population may decline a bit. Maybe even in some years it
recovers. But overall, gradually it slides into local extinction.
Looking backward at the history of a plant population
‘‘going extinct,’’ it may be possible to describe the decay of
such a living dead population. Looking forward, however, it is
much harder to label than is the living dead tree in a cornfield.
After all, all populations have their ups and downs. How to
know, other than retroactively, when a down is a downswing
versus a slide into extinction? When the habitat destruction is
major and obvious, the prediction is much easier, but perhaps
more scientifically trivial, than when the habitat destruction is
piecemeal, fuzzy, or widespread yet light.
What of Animals, Those Things that Move?
ReproductionFthat is, membership in the populationFhas
two components. On the one hand, it is selfevident that the
individual needs to be physiologically able to reproduce. On
the other hand, if it is ecologically neutered, it is as dead as if
sliced off with a chain saw. Selection has not generally favored
the ability of a tree to ‘‘know’’ that it has been ecologically
neutered by the removal of its pollinators, its dispersal agents,
or the safe sites for its juveniles, and then take remedial action.
What would the mutant tree have to be able to do? Walk back
to the forest? Animals, with their chance to move to a new
ecological circumstance, get horny. They search for nesting
sites and mates, they may fight harder for their surviving fewer
children, or they may migrate or emigrate to other places.
But, in the face of the sweeping and omnipresent hand of
humanity, busily extending its extended genome to cover the
globe with both people and their domesticates (Janzen, 1998),
where is the potentially living dead animal to go, and how
long does it have to get there? One can search only so long
before dying of old age, becoming a road kill, or running out
of stored food reserves.
The tropical agroscape, and most wildlands as well, are
awash with living dead animals, animal populations, and
animal arrays (also known as ‘‘communities,’’ whatever those
are). Latent extinction is everywhere, but it operates more
rapidly on animals with their high turnover rate and their
lower capacity for extended lives as dormant seeds, resprout-
ing root stocks, clonal patches, and so on.
Humans contribute in a curious perceptual manner to us
being less aware of the animal living dead. At the level of the
large animals, ‘‘everybody knows’’ that jaguars and tapirs are
still ‘‘here’’ because everyone knows someone who knows
someone who saw one once. One sighting of one 10-year-old
594 Latent Extinction
F
The Living Dead
jaguar crossing the road at noon 12 years ago will sustain the
living dead jaguar in that area for decades, long past its con-
signment to the litter. It has taken more than three decades for
the myth of Costa Rican giant anteaters, which once ranged
these forests, to die a natural death.
Collectors and collections do their part as well. There is a
snapshot of history present in our museum drawers, each
specimen with its neat locality label. These collections con-
tinue the illusion of survival long past the reality. Retroactive
data capture from museums gives a distribution map not of
what is today on the Costa Rican countryside, but rather what
once roamed where today sweeps unbroken waves of sugar-
cane, pasture, plantations, and horticulture. Intellectually
every taxonomist knows this, but the orderly march of speci-
mens across the museum drawers that read Panama, Costa
Rica, Nicaragua, Guatemala, Veracruz, and San Louis Potosı
´
lull one into thinking ‘‘surely over that huge geographic range
there are still viable populations.’’ Plants are not immune to
these processes. It is just that with the more illusive, the
shorter lived, the more mobile, the animal living dead may be
more easily manifest in historical collections than on looking
out the car window at 70 kmph.
And, when one descends from a field vehicle somewhere, a
rare butterfly flutters from the museum drawer and down the
roadside ditch, the cruel illusion is reinforced. Highly mobile
animals are particularly effective at hiding the living dead
from perception. The last living dead Costa Rican green
macaws will fly across the countryside for decades. One small
viable population of butterflies can create hundreds of living
dead individuals searching across the food-plant-free agros-
cape until dying on windshields, of pesticides, or in the col-
lector’s net.
Some animals, like some plants, thrive in the agroscape.
Are they living dead as well? The agroscape changes its biotic
and its physical traits at the whim of some combination of the
market and our technical ability to (re)engineer our do-
mesticates (and produce new ones). Overnight the agroscape
can flip from heaven to hell for a particular species. When
cotton was the crop of choice on the Costa Rican countryside,
the world was an ocean of food for native Dysdercus cotton-
stainer bugs (as well as for a number of other native cotton
herbivores). The local extinction of the bugs’ original wild
food plants (Malvaceae, Sterculiaceae, Bombacaceae) that ac-
companied the forest clearing for cotton fields was invisible.
But when the downstream shrimp industry decided that it
could no longer tolerate the pesticide runoff from the cotton
fields, and cotton went the way of history, then so did the
populations of cotton stainers. Some remain on as tiny (living
dead?) populations on the seeds of local roadside malvaceous
and sterculiaceous herbs, but even these may be living dead
with their food plants easing their slide into extinction.
Does the ecologically neutered tree try harder, as an animal
might? Could there be selection for such behavior? What does
the isolated tree in the field perceive? What is perceived by an
elephant-dispersed tree in a forest where the elephants have
been extinguished? The tree in the field can know that much
less pollen of this or that genetic composition now arrives, and
may adjust accordinglyFit may flower longer, it may set more
seeds that are fertilized with its own pollen. It may make more
flowers more regularly or it may set more wood or grow a
larger crown. All of these things are simple responses to a
circumstance that must occur in a natural forest to this or that
individual that is not living dead. But the extinction of animal
dispersal agents and safe sites for juvenile plants goes un-
heralded, with not even a potential feedback loop.
And What of the Things that Eat the Living Dead?
All have their predators, their parasites, their mutualists, their
scavengers. Many of these are quite dependent on the traits of
their hosts. Food is not food is not food. Narrowly host-
specific specialists abound.
For every living dead individual, population, or species,
there is a large suite of consumersFindividuals, and even
speciesFliving at the margin of their existence. A seed
predator weevilFRhinochenus stigmaFpasses its larval stages
in the pods of guapinol (Hymenaea courbaril) on the Costa
Rican countryside (Janzen, 1974). It maintains what appears
to be a healthy population in the annual to supra-annual fruit
crops that are destined to fall and rot below the parent in the
absence of both the Pleistocene megafauna and the agouti
(Dasyprocta punctata), contemporary inheritor of the guapinol
(Hallwachs, 1986). But as each of those old guapinol trees
dies at the end of its 200 to 500 year life span, the weevil
population takes another hit. One day the last living dead
guapinol trees will die, and along with them will go what
appears today to be a perfectly healthy community of weevils.
The guapinol is also fed on by leaf-eating caterpillars. One,
a large saturniid, Schausiella santarosensis, eats only guapinol
leaves and will go the way of the Rhinochenus weevil. An-
other, Dirphia avia, also a large saturniid, feeds also on the
foliage of Spanish cedar (Cedrela odorata), mahogany (Swiete-
nia macrophylla), oak (Quercus oleoides), and guarea (Guarea
excelsa)(
Janzen and Hallwachs, 2000). As the adult guapinol
trees dwindle in number, how the Dirphia avia population will
twist and change will depend in part on how many indi-
viduals of the other living dead remain. (You guess: How
many Spanish cedar, mahogany and oak trees will be left
standing by the Costa Rican roadside?) Perhaps Guarea excelsa,
its wood of no commercial value, will be the only host plant
left. Enough to sustain Dirphia avia? Who knows, but it cer-
tainly won’t be the same moth population that it was before.
The flowers of the living dead Andira trees were once a
primary food source for tens of thousands of individuals of
hundreds of species of bees; today they are visited by only a
pale shadow of this bee community (Frankie et al., 1998). But
those old adult Andira continue to produce their massive
flower crops and will do so for many decades to come. Its
copious fruits, now largely from pollination by domestic
honey bees, lie rotting below their parents in the absence of
the masses of frugivorous bats that once dispersed them
(Janzen et al., 1976).
As noted earlier, the living dead are a ‘‘natural’’ part of any
plant population. They are those individuals that have fallen
where they have no chance of survival to reproduction. There
are even living dead that have lived past their reproductive age.
However, these living dead differ from the tree in the field in a
very critical way for those who consume them. These living
dead are being continually replenished by the natural
Latent Extinction
F
The Living Dead 595
dispersal process. They do not herald an invisible walk to
extinction for the consumer.
Are There Living Dead Habitats and Ecosystems?
Even when heavily agroindustrialized, the tropical agroscape
often has patches of wildlands (Figure 5)Fforests along rivers
and ravines, broken topography, swamps and marshes, vege-
tation on bad soil, no-man’s land between rival owners,
woodlots, hunting preserves, industrial accidents, parks, and
parklets. This remaining natural vegetation is a patchwork and
a dot map, and it appears to be 1 to 20% of the original
vegetation. And it gives one hope.
One says, ‘‘aha, there are remnants. There is wild bio-
diversity on the countryside, in the agroscape. There is hope
outside of the reserves’’ (which are so hard to maintain and
seem so expensive in national park status). This is a cruel
illusion. Descend to one of these patchlets of forest, so green,
so tree-filled. It is a biodiversity desert, lacking 50 to 99% of its
original biodiversity that it had when it was once part of a
forested landscape. As a package it is a vegetational living
dead. Its species list is a mix of actual living dead and a few
species that can maintain viable populations under these cir-
cumstances. Our major problem is that we visit these patches
as tourists. We were not there in 1965 to see their earlier
biodiversity, to compare it with its pale shadow in 1999 (but
see Frankie et al., 1998).
Why are the survivors living dead, and what happened to
those that have gone locally extinct? Part of them went when
the area got so small that there were no longer circumstances
for a viable population size. Part of them were explicitly mined
or hunted. Part of them went when their mutualists, prey, and
hosts went. Part of them went when the neighboring habitat, a
habitat that spit seeds into the remaining forest and thereby
maintained a population there, went to croplands. Part of
them went when the seasons got drier, or wetter, or windier, or
more fire-rich, or longer, or shorter, or, or, or.
Even those national parks that seem so secure are at major
risk from this phenomenon. When the Southeast Asian dip-
terocarp trees fruit, the wild pigs come from everywhere and
the collective seed crop of the preserved forest patch has no
chance of satiating these seed predators (e.g., Curran et al.,
1999). It may be better to surround a conserved wildland with
wild animal-free rice fields than oceans of secondary suc-
cession subsidizing waves of animals that then turn the small
old-growth forest into yet more secondary succession by
defecating seeds all over it (e.g., Janzen, 1983a).
The bottom line is that the complex fabric woven from
thousands of interacting species has been ripped to bits. Many
of those that seem to have survived are living dead, or the
serendipitous few that find this new impoverished habitat to
their competitive liking. In short, these patches are only
pseudo-remnants, not really smaller pieces of what once was.
Even those ecosystems and habitats that have always existed as
small unitsFa marsh, a landslide scar, a volcano top, a patch
of serpentine soilFdid not live in isolation. Rather, each was
maintained by a complex ebb and flow of immigrants, waifs,
and influences from the neighbors. When the neighboring
natural system is turned to cropland, the integrity of the small
natural patch (e.g., Figure 5) is usually trashed almost as badly
as if an army of chain saws had run through it. It just takes a
bit longer for the living dead to live out their physiological
lives.
These impoverished patches are especially deceptive
for the bioilliterate. For those to whom a forest is just a batch
of large woody plants, for those who cannot or will not read
the differences between an advertising ditty and a complex
poem, the agroscape with its living dead and pseudo-remnant
natural vegetation appears to be not much different from a
glade and forest mix in a national park. All seems to be well.
But when humanity expects something from that wildland
patch, it discovers that almost all of its tropical biodiversity
is gone.
These patches have also played a mean trick on the con-
servation community. A huge portion of the world’s conser-
vation policy is based on the understandings of nature held
largely intuitively by those who have grown up extra-tropical
and learned their lessons from extra-tropical ecosystems. They
easily adopt the mantra of trying to save the biodiversity
remnants scattered across the agroscape. They are especially
prone to do so in the face of the frustration of trying to save
very large (and commercially juicy) blocks of intact vegetation.
The forest-patchlet-dotted agroscape of Minnesota or Sweden
still collectively contains easily more than 80% of the species
that were there when the European colonists arrived. However,
the same snapshot of a Costa Rican agroscape contains at best
5 to 20% of what once was. And the percent is still falling
rapidly because a huge fraction of what remains today is living
dead.
The more biodiverse and the more complex an ecosystem,
the more likely that human perturbation will create anthro-
pogenic living dead among the species with longer-lived in-
dividuals. This is because perturbations strip away mutualists
and other biointeractors, leaving behind the physiologically
functional individuals to live out their neutered life spans.
The more biodiverse and the more complex, the more likely
Figure 5 A living dead patch (left center) of natural vegetation,
composed primarily of living dead individuals, among rice fields.
There is essentially no gene flow between the patch and the
secondary successional wildland in the foreground despite the thin
connecting strip of riparian vegetation. Southwest of Liberia,
Guanacaste Province, Costa Rica, December 14, 1999.
596 Latent Extinction
F
The Living Dead
any given individual is to be dependent on one or more of
these interactants to remain a member of the population.
This tropical-to-extra-tropical comparison, derived by
spending my life peering closely at both tropical and extra-
tropical habitats is a major driver behind the conclusion
that in the tropics a triage decision is needed. The living
dead are writhing in lethal pain on the battlefield of the tro-
pical agroscape. If we expend our scarce financial, political,
and social resources on them instead of saving a few large
coherent blocks of multi-ecosystem biophysical units, in the
end we will live an even yet more impoverished biodiversity
existence.
The future of real conservation in the tropics lies in by-and-
large focusing our efforts on the survival of a relatively small
number of very large and diverse biophysical units, each
complicatedly integrated with local, national, and inter-
national societies (Janzen, 1998, 1999). Painful as it may be,
resources spent on trying to save individual species and small
habitat fragments scattered across the agroscape, often living
dead, is bad conservation economics and creates an angry
antagonistic Homo sapiens.
We have no option in the tropics but to recognize that
conserved wildlands are and always will be islands in an ocean
of agroscape. Our task is to get on with rendering them into
the highest quality islands possible, and not be distracted by,
nor lulled by, the living dead individuals and islandlets. Yes, if
there remains but just one Rembrandt painting, we of course
save it even if it is bullet-holed and faded. However, we must
recognize it for what it is and not convince ourselves that by
doing so we have preserved our knowledge of European
history.
Restoration Biology
The living dead are largely a negative force in the algebra of
conservation biology and conservation reality. However, in
those few cases where ecosystem restoration is desired or ser-
endipitous, their life span delimits a window of opportunity
for the reintegration of their species into the restoring eco-
system. Reintegration is not an unqualified given, however.
A single large tree in a pasture being restored to forest may be
dropping its seeds and fruits into an early successional old-
field community that for decades is still way too unattractive
to contain the seed dispersal coterie that will begin to restore
the demography of that tree species. Equally, the pollinators of
its flowers may already be extinct, or abhor the young sec-
ondary succession coming up below the large old parent. And
finally, the physical climate of the highly deciduous and dry-
season blasted secondary succession may well be a dismal
place for a seedling or sapling of that old-growth giant. As
every plantation initiator knows, the act of stuffing seeds into
the ground does not a plantation make.
Until a very short time ago, the California condor was
made up of living dead individuals. They were brought into
captivity (e.g., transplanted to a safe field), reproduced (e.g.,
seeds collected and grown in pots), and have been put back
out, hopefully in an agroecosystem with a friendly sociology.
This habitat is, however, very seriously impoverished through
reduction of marine mammal populations that so kindly
generated the cadavers for lunch, and the California condor
may always be dependent on human subsidy.
Many species of living dead may be rescued in this manner,
if we care enough to spend the resources on them and
gather information about them. But before racing out to
apply the same technique to the living dead guapinol trees in
the centers of Costa Rican pastures, a question very much
needs to be addressed. Would not the same money spent
on saving large blocks of guapinol-occupied wildlands, com-
plete with their pollinators and dispersal agents, not generate
vastly more conservation of guapinol and its hundreds of
thousands of compatriot species? Yes, even these large blocks
of wildland will contain some living dead. The wildland’s
biodiversity will attain an equilibrium density at whatever
number of species survive the reduction from a continent of
wildland to a large island of wildland. Those who are extin-
guished during this process will suggest the list of who were
the living dead.
See also: Central America, Ecosystems of. Conservation Biology,
Discipline of. Deforestation and Land Clearing. Forest Ecology.
Mammals (Late Quaternary), Extinctions of. Modern Examples of
Extinctions. Pollinators, Role of. Range Ecology, Global Livestock
Influences. Restoration of Biodiversity, Overview. Tropical Forest
Ecosystems
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... For plants, this lag time may last several centuries. This phenomenon is illustrated by the fact that in highly degraded ecosystems, such as agricultural areas where the native forest has been cleared, for instance in Costa Rica (Janzen, 2001), individual indigenous trees may survive for decades although there is no recruitment; these trees were called "the living dead" by Janzen (2001). This lag time is usually much longer in plants than in animals because (i) many plants have longer lifespans than animals, (ii) the presence of a soil seed bank that may produce individuals until it is exhausted, and (iii) many plants can reproduce asexually, which allows the last individual to produce successors. ...
... For plants, this lag time may last several centuries. This phenomenon is illustrated by the fact that in highly degraded ecosystems, such as agricultural areas where the native forest has been cleared, for instance in Costa Rica (Janzen, 2001), individual indigenous trees may survive for decades although there is no recruitment; these trees were called "the living dead" by Janzen (2001). This lag time is usually much longer in plants than in animals because (i) many plants have longer lifespans than animals, (ii) the presence of a soil seed bank that may produce individuals until it is exhausted, and (iii) many plants can reproduce asexually, which allows the last individual to produce successors. ...
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Hymenaea courbaril (guapinol) is a large-seeded neotropical tree that owes much of its present widespread distribution to seed dispersal by agoutis. Guapinol fruit and fruiting traits influence the fate of a pod’s seeds by affecting agouti scatterhoarding behavior. Agoutis transport pods of experimental fruit crops 0−200+ m. In Costa Rican lowland dry forest, the distance a pod is carried and the rate pods are removed from a crop are strongly influenced by season and by the condition of a pod’s fruit pulp. In turn, distance strongly affects seed survival: near the parent tree, where guapinol seeds and other foods are concentrated, 99% of seeds and seedlings are killed by peccaries, agoutis and mice. However, where guapinol seeds and other foods are at a low density, mortality of buried seeds and seedlings is about 50%. Likewise, pods left below the parent tree are in danger of being opened by seed-crushing collared peccaries and, until the last few decades, white-lipped peccaries. Agouti scatterhoarding is the only process that moves Santa Rosa guapinol seeds from zones of very high seed-seedling mortality to zones of lower mortality. In the absence of agoutis, guapinol would probably be locally extinct wherever peccaries and guapinol-eating small rodents were common. However, the present interaction between guapinol and its seed predators and dispersers is serendipitous rather than coevolved: guapinol fruit traits probably have changed little since they evolved in the Oligocene among a species-rich fauna of large herbivorous dispersal agents. Since the Pleistocene megafaunal extinctions, guapinol’s survival in much of its range may have been due to the possession of fruit traits that allowed successful seed dispersal by agoutis. Similarly, agoutis now disperse the seeds of other largeseeded or hard-fruited tree species whose fruit and seed traits presumably evolved in part as a consequence of megafaunal seed dispersal. These plant species possess two traits. The seeds must be eaten by agoutis, and must be sufficiently protected to survive the slow process of agouti scatterhoarding. Agoutis (the largest scatterhoarders of seeds) surpass all other extant neotropical mammals in dispersing large seeds and seeds from hard fruits, because the upper size limit to dispersal is set by what scatterhoarders can lift rather than what they can swallow, and because they gnaw rather than crush open fruits. Dispersal patterns, and hence the genetic structure of tree populations, must have changed greatly when territorial scatterhoarding rodents took over the dispersal of guapinol and other trees from seed-swallowing megaherbivores. The two species of peccaries, which are as widespread as are agoutis, overlap with agoutis extensively in diet but kill rather than disperse large seeds. They are parasites of many of the agoutimegafauna-flora interactions.
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Daniel Janzen is an ecologist specializing in tropical animal-plant interactions, wildland biodiversity management, and the human-nature interface, interests that he shares with his ecologist wife Winnie Hallwachs. He is Professor of Biology at the University of Pennsylvania and Technical Advisor to