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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
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.
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
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
When the terrestrial world was covered with forest eco-
systems, the single tree left standing in an aboriginal cornfield
Encyclopedia of Biodiversity, Volume 4
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,
Latent Extinction
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
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
Guanacaste, May 28, 1988.
592 Latent Extinction
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
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
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
The Living Dead 593
dead, there can be no natural selection inflicted on the food
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
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
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
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
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
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
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
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
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
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
Aldrich PR and Hamrick JL (1998) Reproductive dominance of pasture trees in a
fragmented tropical forest mosaic. Science 281: 103–105.
Curran LM, Caniago I, Paoli GD, Astianti D, Kusneti M, Leighton M, Nirarita CE,
and Haeruman H (1999) Impact of El Nin
˜o and logging on canopy tree
recruitment in Borneo. Science 286: 2184–2188.
Frankie GW, Vinson SB, Rizzardi MA, Griswold TL, O’Keefe S, and Snelling RR
(1998) Diversity and abundance of bees visiting a mass flowering tree species
in disturbed seasonal dry forest, Costa Rica. Journal of the Kansas
Entomological Society 70: 281–296.
Hallwachs W (1986) Agoutis (Dasyprocta punctata): The inheritors of guapinol
(Hymenaea courbaril: Leguminosae). In: Estrada A and Fleming T (eds.)
Frugivores and Seed Dispersal, pp. 285–304. Dordrecht: Dr. W. Junk Publishers.
Janzen DH (1974) The deflowering of Central America. Natural History 83:
Janzen DH (1981) Enterolobium cyclocarpum seed passage rate and survival in
horses, Costa Rican Pleistocene seed dispersal agents. Ecology 62: 593–601.
Janzen DH (1982a) Differential seed survival and passage rates in cows and horses,
surrogate Pleistocene dispersal agents. Oikos 38: 150–156.
Janzen DH (1982b) How and why horses open Crescentia alata fruits. Biotropica
14: 149–152.
Janzen DH (1983a) No park is an island: increase in interference from outside as
park size decreases. Oikos 41: 402–410.
Janzen DH (1983b) The pleistocene hunters had help. American Naturalist 121:
Janzen DH (1984) Dispersal of small seeds by big herbivores: Foliage is the fruit.
American Naturalist 123: 338–353.
Janzen DH (1985) On ecological fitting. Oikos 45: 308–310.
Janzen DH (1986a) The eternal external threat. In: Soule ME (ed.) Conservation
Biology: The Science of Scarcity and Diversity, pp. 286–303. Sunderland, MA:
Sinauer Associates.
Janzen DH (1986b) The future of tropical ecology. Annual Review of Ecology and
Systematics 17: 305–324.
Janzen DH (1986c) Lost plants. Oikos 46: 129–131.
Janzen DH (1998) Gardenification of wildland nature and the human footprint.
Science 279: 1312–1313.
Latent Extinction
The Living Dead 597
Janzen DH (1999) Gardenification of tropical conserved wildlands: Multitasking,
multicropping, and multiusers. PNAS 96(11): 5987–5994.
Janzen DH and Hallwachs W (2000) Philosophy, navigation and use of a dynamic
database (‘‘ACG Caterpillars SRNP’’) for an inventory of the macrocaterpillar
fauna, and its food plants and parasitoids, of the Area de Conservacio
Guanacaste (ACG), Northwestern Costa Rica.(
Janzen DH and Martin PS (1982) Neotropical anachronisms: The fruits the
gomphotheres ate. Science 215: 19–27.
Janzen DH, Miller GA, Hackforth-Jones J, Pond CM, Hooper K, and Janos DP
(1976) Two Costa Rican bat-generated seed shadows of Andira inermis
(Leguminosae). Ecology 56: 1068–1075.
598 Latent Extinction
The Living Dead
... 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. ...
Full-text available
There have been five Mass Extinction events in the history of Earth's biodiversity, all caused by dramatic but natural phenomena. It has been claimed that the Sixth Mass Extinction may be underway, this time caused entirely by humans. Although considerable evidence indicates that there is a biodiversity crisis of increasing extinctions and plummeting abundances, some do not accept that this amounts to a Sixth Mass Extinction. Often, they use the IUCN Red List to support their stance, arguing that the rate of species loss does not differ from the background rate. However, the Red List is heavily biased: almost all birds and mammals but only a minute fraction of invertebrates have been evaluated against conservation criteria. Incorporating estimates of the true number of invertebrate extinctions leads to the conclusion that the rate vastly exceeds the background rate and that we may indeed be witnessing the start of the Sixth Mass Extinction. As an example, we focus on molluscs, the second largest phylum in numbers of known species, and, extrapolating boldly, estimate that, since around AD 1500, possibly as many as 7.5-13% (150,000-260,000) of all~2 million known species have already gone extinct, orders of magnitude greater than the 882 (0.04%) on the Red List. We review differences in extinction rates according to realms: marine species face significant threats but, although previous mass extinctions were largely defined by marine invertebrates, there is no evidence that the marine biota has reached the same crisis as the non-marine biota. Island species have suffered far greater rates than continental ones. Plants face similar conservation biases as do invertebrates, although there are hints they may have suffered lower extinction rates. There are also those who do not deny an extinction crisis but accept it as a new trajectory of evolution, because humans are part of the natural world; some even embrace it, with a desire to manipulate it for human benefit. We take issue with these stances. Humans are the only species able to manipulate the Earth on a grand scale, and they have allowed the current crisis to happen. Despite multiple conservation initiatives at various levels, most are not species oriented (certain charismatic vertebrates excepted) and specific actions to protect every living species individually are simply unfeasible because of the tyranny of numbers. As systematic biologists, we encourage the nurturing of the innate human appreciation of biodiversity, but we reaffirm the message that the biodiversity that makes our world so fascinating, beautiful and functional is vanishing unnoticed at an unprecedented rate. In the face of a mounting crisis, scientists must adopt the practices of preventive archaeology , and collect and document as many species as possible before they disappear. All this depends on reviving the venerable study of natural history and taxonomy. Denying the crisis, simply accepting it and doing nothing, or even embracing it for the ostensible benefit of humanity, are not appropriate options and pave the way for the Earth to continue on its sad trajectory towards a Sixth Mass Extinction.
... Anthropogenic loss of natural habitat is a widespread phenomenon of the anthropocene. A large proportion of terrestrial land area has been converted to what Janzen (2001) called "agroscape" (i.e., the agricultural landscape of ranches, plantations, and crop fields, along with associated infrastructure of roads, buildings, and drainage or irrigation ditches). In this agroscape, relict wildland trees often exist as non-viable populations or single non-reproducing individuals that Janzen has called the "living dead" (Janzen, 2001). ...
... A large proportion of terrestrial land area has been converted to what Janzen (2001) called "agroscape" (i.e., the agricultural landscape of ranches, plantations, and crop fields, along with associated infrastructure of roads, buildings, and drainage or irrigation ditches). In this agroscape, relict wildland trees often exist as non-viable populations or single non-reproducing individuals that Janzen has called the "living dead" (Janzen, 2001). In addition to the agroscape, there has been an increase in degraded land (wildland with decreased biodiversity due to resource extraction, introduced biota, erosion, or desertification). ...
Full-text available
The flora of the island of St Helena provides an amplified system for the study of extinction by reason of the island’s high endemism, small size, vulnerable biota, length of time of severe disturbance (since 1502), and severity of threats. Endemic plants have been eliminated from 96.5% of St Helena by habitat loss. There are eight recorded extinctions in the vascular flora since 1771 giving an extinction rate of 581 extinctions per million species per year (E/MSY). This is considerably higher than background extinction rates, variously estimated at 1 or 0.1 E/MSY. We have no information for plant extinctions prior to 1771 but applying the same extinction rate to the period 1502–1771 suggests that there may be around 10 unrecorded historical extinctions. We use census data and population decline estimates to project likely extinction forward in time. The projected overall extinction rate for the next 200 years is somewhat higher at 625 E/MSY. However, our data predict an extinction crunch in the next 50 years with four species out of the remaining 48 likely to become extinct during this period. It is interesting that during a period when the native plant areas dropped to 3.5% of the original, the extinction rate appears to have remained shallowly linear with under 30% of the endemic flora becoming extinct.
... However, the functioning of ecological processes also depends on the number of individuals that fulfil certain functional roles, that is, on abundance itself Winfree et al., 2015), and these individuals can be composed of different but functionally similar species. Given that many species in tropical networks have low local abundances that are limited by factors other than the availability of food (Hubbell, 2013), the loss of species with apparently redundant roles or even the reduction in the number of individuals fulfilling these roles could have detrimental effects on plant communities (Dee et al., 2019;Gaston & Fuller, 2008;Janzen, 2001;Rosenberg et al., 2019;Valiente-Banuet et al., 2015). Unfortunately, interaction networks are usually not sufficiently well-resolved to investigate the effect of the number of individuals per species that participate in the network. ...
Species differ in their resource use and their interactions with other species and, consequently, they fulfil different functional roles in ecological processes. Species with specialized functional roles (specialists) are considered important for communities because they often interact with species with which few other species interact, thereby contributing complementary functional roles to ecological processes. However, the contribution of specialists could be low if they only interact with a small range of interaction partners. In contrast, species with unspecialized functional roles (generalists) often do not fulfil complementary roles but their contribution to ecological processes could be high because they interact with a large range of species. To investigate the importance of the functional roles of specialists versus generalists, we tested the relationship between species’ degree of specialization and their contribution to functional‐role diversity for frugivorous birds in Andean seed‐dispersal networks. We used two measures for the specialization of birds—one based on the size, and one based on the position of their interaction niche—and measured their effect on the birds’ contribution to functional‐role diversity and their functional complementarity, a measure of how much a species’ functional role is complementary to those of the other species. In all networks, there were similar log‐normal distributions of species’ contributions to functional‐role diversity and functional complementarity. Contribution to functional‐role diversity and functional complementarity increased with both increasing niche‐position specialization and increasing niche size, indicating that the composition of functional roles in the networks was determined by an interplay between specialization and generalization. There was a negative interaction between niche‐position specialization and niche size in both models, which showed that the positive effect of niche‐position specialization on functional‐role diversity and functional complementarity was stronger for species with a small niche size, and vice versa. Our results show that there is a continuum from specialized to generalized functional roles in species communities, and that both specialists and generalists fulfil important functional roles in ecological processes. Combining interaction networks with functional traits, as exemplified in this study, provides insight into the importance of an interplay of redundancy and complementarity in species’ functional roles for ecosystem functioning.
... These pressures from loss of habitat and fragmentation lead to the extinction of some species. Many species now survive at such low densities that they can be considered nearly functionally extinct (Janzen 2001). Specialist species with narrow feeding niches may be less likely to make use of resources in the habitats that surround fragments than generalist species with broad feeding niches (Lees and Peres 2008, Vetter et al. 2011, Newbold et al. 2012, Olivier and Van Aarde 2017. ...
Establishing the specific habitat requirements of forest specialists in fragmented natural habitats is vital for their conservation. We used camera-trap surveys and microhabitat-scale covariates to assess the habitat requirements, probability of occupancy and detection of two terrestrial forest specialist species, the Orange Ground-thrush Geokichla gurneyi and the Lemon Dove Aplopelia larvata during the breeding and non-breeding seasons of 2018-2019 in selected Southern Mistbelt Forests of KwaZulu-Natal and the Eastern Cape, South Africa. A series of camera-trap surveys over 21 days were conducted in conjunction with surveys of microhabitat structural covariates. During the wet season, percentage of leaf litter cover, short grass cover, short herb cover, tall herb cover and saplings 0-2 m, stem density of trees 6-10 m and trees 16-20 m were significant structural covariates for influencing Lemon Dove occupancy. In the dry season, stem density of 2-5 m and 10-15 m trees, percentage tall herb cover, short herb cover and 0-2 m saplings were significant covariates influencing Lemon Dove occupancy. Stem density of trees 2-5 m and 11-15 m, percentage of short grass cover and short herb cover were important site covariates influencing Orange Ground-thrush occupancy in the wet season. Our study highlighted the importance of a diverse habitat structure for both forest species. A high density of tall/mature trees was an essential microhabitat covariate, particularly for sufficient cover and food for these ground-dwelling birds. Avian forest specialists play a vital role in providing ecosystem services perpetuating forest habitat functioning. Conservation of the natural heterogeneity of their habitat is integral to management plans to prevent the decline of such species.
... Human colonization and the associated introduction of mammalian predators has resulted in dramatic changes for many island ecosystems, leading to unprecedented biodiversity loss (Blackburn, Cassey, Duncan, Evans, & Gaston, 2004;Wood et al., 2017). More than 80% of the documented terrestrial species extinctions since 1600 CE have been island endemics (Groombridge, 1992), and many extant island species have been so severely reduced in abundance that they can be considered functionally extinct (Janzen, 2001;McConkey & O'Farrill, 2015). ...
1. Human colonization of islands has resulted in the reduction or loss of many native species, and the introduction of non-native species, producing novel ecosystems. The impacts of these changes on mutualistic plant-animal interactions have received considerable attention, but the potential effects on some antagonistic interactions, such as seed predation, are less thoroughly understood, and often overlooked. 2. Using three archetypal island groups-New Zealand, the Mascarenes and Hawaiʻi-we compare the taxonomic richness and functional diversity of vertebrate seed predators from prehuman and contemporary ecosystems. We scored species on several traits relevant to seed predation, then clustered species into functionally similar groups using hierarchical clustering. 3. These archipelagos once supported between 19 and 24 species of exclusively avian seed predators (representing two to four orders) ranging from large, flight-less herbivores to small, volant finches and parrots. Following human arrival, 63%-89% of these species went extinct, and between 12 and 23 non-native seed predators were introduced. Contemporary seed predator faunas consist of between 14 and 26 species (representing six to seven orders), dominated by non-native granivorous birds and omnivorous mammals. 4. Our results reveal several examples in which non-native species may be functionally similar to extinct seed predators, but most non-native species are functionally different from extinct species, and therefore may be introducing novel seed predation pressures for insular ecosystems. Mammalian seed predators are especially functionally different from the native avian seed predators, as their teeth and widespread habitat distribution allow them to destroy a more diverse range of seeds, including the largest seeds.5. We highlight the need to understand how these altered seed predator communities are affecting native plant populations, particularly in the context of reduced pollination and seed dispersal. More broadly, we argue that antagonistic interactions are an integral part of any ecosystem, and therefore must be understood if we are to achieve more holistic restoration frameworks for insular ecosystems.
... Our findings suggest that genetic factors are unlikely to be the direct cause of the observed decline in small populations of adders. Instead, small populations may already be "doomed to extinction by demographic factors before genetic effects act strongly" [93], representing the "living dead" [94,95], where continuation of a population or metapopulation becomes demographically impossible. For example, the reproductive ecology of adders renders small populations profoundly vulnerable to stochastic sex bias [96][97][98]. ...
Full-text available
Genetic factors are often overlooked in conservation planning, despite their importance in small isolated populations. We used mitochondrial and microsatellite markers to investigate population genetics of the adder (Vipera berus) in southern Britain, where numbers are declining. We found no evidence for loss of heterozygosity in any of the populations studied. Genetic diversity was comparable across sites, in line with published levels for mainland Europe. However, further analysis revealed a striking level of relatedness. Genetic networks constructed from inferred first degree relationships suggested a high proportion of individuals to be related at a level equivalent to that of half-siblings, with rare inferred full-sib dyads. These patterns of relatedness can be attributed to the high philopatry and low vagility of adders, which creates high local relatedness, in combination with the polyandrous breeding system in the adder, which may offset the risk of inbreeding in closed populations. We suggest that reliance on standard genetic indicators of inbreeding and diversity may underestimate demographic and genetic factors that make adder populations vulnerable to extirpation. We stress the importance of an integrated genetic and demographic approach in the conservation of adders, and other taxa of similar ecology.
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Human‐modified forests—HMFs—now cover more area worldwide than primary forests and could help buffering the ongoing species loss. However, their role in protecting canopy epiphytes remains unclear, partially because these communities require large trees, high humidity, and shade, conditions which are rare in HMFs. Here, we assessed how canopy epiphytes, in different ontogenetic stages, are structured in HMFs. Specifically, we evaluated how species richness, total abundance, and community composition, and how abundance of seedlings and juveniles, are affected by the local and landscape context in the Atlantic Forest of Brazil. Across all sites, we found 82.9% of species and 75.5% of individuals exclusively in old‐growth forest, while HMFs hosted only 15.5% of all species, sharing 75% of their species with old‐growth forests communities, and pastures hosted 1% of species richness and 2.8% of individuals sharing 60% of their species with old‐growth forest communities. We also found that seedling and juveniles were twice as abundant than adults in old‐growth forest, similarly abundant to adults in HMFs and absent from pastures. Low numbers of individuals in early ontogenetic stages in HMFs and pastures are likely to impact future generations of epiphytes in these areas. Although HMFs provide important refuge for many species, our results show that they do not provide suitable conditions for the maintenance of current or future canopy epiphyte communities. Our findings suggest that conserving large continuous old‐growth forests is the only viable conservation option for protecting most vascular epiphytes. Abstract in Portuguese is available with online material. Atualmente, florestas modificadas pelo homem—FMHs—cobrem mais área em todo o mundo do que florestas primarias e poderiam ajudar a conter a atual perda de espécies. Porém, seu papel na preservação de epífitas de dossel permanece incerto, parcialmente porque esas comunidades requerem sombra, árvores grandes e alta umidade, condições raras em FMHs. No presente estudo, avaliamos como as epífitas de dossel, em diferentes estágios ontogenéticos, estão estruturadas em FMHs. Especificamente, avaliamos como a riqueza de espécies, a abundância total e composição da comunidade, assim como a abundância de plântulas e de juvenis, são afetadas pelo contexto local e paisagístico em florestas da Mata Atlântica do Brasil. Em todos os locais, encontramos que 82.9% das espécies, e 75.5% dos indivíduos, foram exclusivas das florestas primarias. FMHs apresentaram apenas 15.5% da riqueza total de espécies, compartilhando 75% destas espécies com comunidades de florestas maduras. Pastagens tiveram 1% de riqueza total espécies e 2.8% do total de indivíduos, compartilhando 60% de suas espécies com comunidades florestais maduras. Em florestas maduras, plântulas e juvenis foram duas vezes mais abundantes do que adultos; em FMHs a abundância de plântulas e juvenis foi similar à de adultos; e em pastagens não houve presença de plântulas ou juvenis. O baixo número de indivíduos nos primeiros estágios ontogenéticos as FMHs e nas pastagens provavelmente pode prejudicar as futuras gerações de epífitas nessas áreas. Embora as FMHs forneçam refúgio para muitas espécies nativas, nossos resultados indicam que elas não fornecem condições apropriadas para a manutenção de comunidades epifíticas atuais ou futuras. De acordo com nossos resultados, a conservação de grandes áreas contínuas de floresta primaria é a única opção viável para proteger a maioria das comunidades epifíticas vasculares de dossel Although HMFs provide important refuge for many species, our results show that they do not provide suitable conditions for the maintenance of current or future canopy epiphyte communities. Our findings suggest that conserving large continuous old‐growth forests is the only viable conservation option for protecting most vascular epiphytes.
Forecasting how climate change will impact biological systems represents a grand challenge for biologists. However, climate change biology lacks an effective framework for anticipating and resolving uncertainty. Here, we introduce the concept of climate change wildcards: biological or bio‐climatic processes with a high degree of uncertainty and a large impact on our ability to address the biotic consequences of climate change. Wildcards may occur at multiple points in the progression of research — from understanding, to predicting, to forecasting biological responses. Our understanding of biological responses is limited by the components and processes we exclude to make research tractable. Our ability to predict biological responses often requires integration between biological levels of organization, across multiple stressors, and from specific cases to general systems. However, these types of integration can be dramatically affected by, respectively, differences between biological levels in their critical points, non‐additivity of the effects of different stressors, and historical and geographic contingency. Finally, our ability to forecast biological responses to climate change requires incorporating climatic projections in bio‐climatic models. Such forecasts are vulnerable to the compounding of biological and climatic uncertainty, especially when biological responses occur in novel areas of bio‐climatic parameter space. Both biological responses and climate change are dynamic processes; the potential of biological systems to be buffered against or rescued from the effects of climate change depends on the relative timing of biological and climatic effects ‐ one of the least predictable aspects of both systems. In sum, our framework identifies stress points in the research process where we should anticipate and forestall wildcards. Focusing on universal currencies, like energy and elements, and universal structures, like functional traits and ecological networks, will improve our ability to generalize results. Most importantly, by modelling and communicating uncertainty, climate change biology can identify critical foci for future research.
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I have been watching the gradual and very visible decline of Mexican and Central American insect density and species richness since 1953 and Winnie since 1978. The loss is very real for essentially all higher taxa, and the reasons are very evident: intense forest and agricultural simplification of very large areas, massive use of pesticides, habitat fragmentation, and at least since the 1980's, ever-increasing climate change in temperature, rainfall, and synchronization of seasonal cues. There is no ecological concept suggesting that this biodiversity and habitat impoverishment is restricted to this portion of the Neotropics, and our 50 years of occasional visits to other parts of the tropics suggest the same. We are losing most of the insect community that is still in the cloud forests due to the drying of the tops of tropical mountains, just as we are losing the huge expanses of insect communities that once occupied the fertile soils, weather, and water of the lowland tropics. Today we have unimaginable access to the world's biodiversity through the internet, roads, dwellings, education, bioliterate societies, DNA barcoding, genome sequencing, and human curiosity. The wild world gains from our understanding that it needs large and diverse terrain, relief from hunting trees and animals, site-specific restoration, profit-sharing with its societies, and tolerance of humans and our extended genomes. But if our terrestrial world remains constructed through constant war with the arthropod world, along with the plants, fungi and nematodes, human society will lose very big time. The house is burning. We do not need a thermometer. We need a fire hose.
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Chronic herbivory by elephants rarely eliminates any species of woody savanna plants because these plants are typically vigorous basal resprouters after damage by fire or herbivory. In some instances, resprouting after elephant herbivory even increases stem numbers per unit area compared to protected areas. It is thus difficult to know whether an area has been severely degraded by elephant herbivory or not because although trees may be severely reduced in size, they will still be present and may even be relatively dense. By using an elephant exclosure in the Kruger National Park, South Africa, we demonstrate that this resprouting ability masks the fact that entire populations of a widespread African palm, Hyphaene petersiana, are prevented from reaching sexual maturity by chronic elephant herbivory. Besides sterilizing these palms and thus preventing their evolution and seed dispersal, the absence of the palm fruits, flowers and tall stems has other negative biodiversity impacts on their associated fauna. We suggest that to determine sustainable elephant impacts on savanna plants, conservation managers also use the reproductive condition of savanna plants rather than their presence, height or stem density.
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Costa Rican horses ranging free in deciduous forest-grassland habitats swallow about half of the seeds in the Enterolobium cyclocarpum fruits that they eat, and six such horses defecated at least 9-56% of the seeds alive. While about three-quarters of the surviving seeds appeared by the 14th d after ingestion, about a quarter of the surviving seeds emerged 15-60 d after ingestion. The horse kills Enterolobium seeds by digestive processes shortly after the seed germinates in response to the moisture of the intestinal tract. More than 90% of the seeds that survived the trip did so as hard dormant seeds. They showed no indication that they would germinate more rapidly (break dormancy more rapidly) that seeds planted directly from the fruits. The horse-seed interaction suggests that Pleistocene horses may have contributed to both local and long-distance population recruitment by Enterolobium cyclocarpum, and contemporary horses certainly have the potential to do so.
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Two female Costa Rican range cattle were fed 961 and 1407 large hard dormant seeds of the guanacaste tree Enterolobium cyclocarpum. Of the 823 and 1111 hard dormant seeds defecated, 66 and 86% had emerged by the end of the fifth day and 87 and 96% had emerged by the end of the tenth day. By day 10, three range horses had defecated only 45, 50 and 71% of the hard guanacaste seeds they would defecate. Compared with that of the cows, the daily distribution of seeds defecated by the horses had a proportionately lower peak, was proportionately much more skewed to the right and contained many days on which no seeds were defecated. The cows killed a maximum of 14-21% of the seeds that they swallowed while the horses killed 44-83%. A lower proportion of the seeds defecated by the cows were soft (dead or alive) than was the case with the horses, one cow did not defecate heavier seeds at a different rate than it defecated lighter seeds, and one cow produced highly variable numbers of seeds per dung pile each day. Given the working hypothesis that the large caecum of the horse selectively takes large seeds out of the flow of digesta and later puts them back into it in pulses as it cleans the caecum, I hypothesize that the differences between the cow and horse in the manner of defecating guanacaste seeds is due to the much smaller caecum of the cow not acting in this manner. Additionally, a horse chews and sorts its food more carefully at first intake than does a cow with respect to large hard objects; this may be in part due to the danger to a horse of a caecum obstructed by such objects. /// двум коровам местного Коста-Риканского скота скормили 961 и 1407 крупных твердых сенян дерева гуанакасты (Entecolobium cyelocorpum). Из 823 и 1111 семян, выброшенных с фекалиями, 66 и 86% найдено к концу пятого дня и 87 и 96% - к концу десятого дня. К десятому дню три местные лошади выборосили лишъ 45, 50 и 71% от общего количества твепдых семян гыанакасты, удаленных с фекалиями. В сравнении с коровами, кривая ежедневного количества семян, выбрасываемых с фекалиями, у лошадей имеет пропорционалъно более низкий пик и болъше уклоняется вправо, a таюже насчитывает менъшее количество дней, когда выбрасываются семена. у коров погибает максимум 14-21% заглатываемых семян, a y лошадей - 44-83%. Менъшая частъ семян, выбрасываемых коровами, размитчена (мертвые и живые сенена), чем зто наблюдалосъ у лошадей; коровы не выбрасывают более тяжелые семена с яной скоростъю, нежели более легкие; ы них ежедневно выбрасывается разное количество семян в отделъных лепешках. Приняв рабочую гипстезу, что в слепой кишке у лошадей селективно задерживаются крупнные семена из потока переваренной пищи, а затем снова импулъсивно выбрасываются в зтот поток при прочистке слепой, кишки, я предполагаю, что различия ы коров и лошадей б дефекации семян гуанакасты определяытчя что гораздо менъшая по размерам млепая кишка коров не функционирует таким образом. Кроме того, лошадъ пережевывает и сортирует пишу более тщателъно при заглатывании, чем корова, имея в виду, что зто - оченъ крупнные и твердые пищевые объекты. Это частично может объяснятъся опасностъю для лошадей засорения слепой кишки крупныни твердыми пищевыми объектами.
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Bat-generated seed shadows of two mature Andira inermis (W. Wright) DC. trees in the deciduous forest lowlands of Guanacaste Province, Costa Rica, are highly heterogeneous; very unequal numbers of seeds are deposited beneath the trees used as feeding roosts. It is calculated that a 45-g Artibeus jamaicensis bat may potentially obtain as many as 1,766 joules [= 422 calories] per Andira fruit per round trip of 270 m between the parent tree and the feeding roost. Seed predation by Cleogonus weevils was found to be highest below the parent tree, intermediate under bat feeding roosts, and lowest among fruits dropped accidentally by bats between the parent tree and the feeding roosts.
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There is evident conservation value to numerous small habitat preserves (parks) when large protected areas are impractical (Simberloff 1982). However, such a management policy brings to mind a caution that is often unappreciated for parks and other forms of conserved pristine vegetation, and becomes ever more appropriate as park size decreases. The smaller the patch (island) of habitat that is viewed as pristine, the greater the effect of the surrounding secondary successional vegetation and croplands as a source of 1) animals and seeds that enter the park and interact with the residents, and 2) food subsidy for residents capable of foraging outside of the pristine forest.
Loss of habitat is one of the primary reasons for loss of species and for overall reduction in biodiversity, including the recent decline of pollinating insect populations. Comparison of systematic samples of bees attracted to a mass flowering tree, Andira inermis (Fam. Fabaceae), in 1972 and 1996 at Liberia, a site in the seasonal dry forest of Guanacaste Province, Costa Rica. Indicated a significant reduction of bee pollinators due to habitat loss over the 24 year period. In 1972, about 70 bee species were collected from trees of A. inermis at Liberia. In 1996, only 28 species were collected, and their frequencies were substantially lower. Overall the 1996 sample represented a reduction of 90% in total bees collected. Samples collected during the same season at a second less disturbed site, Monteverde, were both higher in numbers of species (37) and in numbers of bees than the Liberia collections. Loss of habitat due to agricultural development and other human-disturbances such as fire are discussed as the primary reasons for the loss of bee species richness and abundance at the two study sites. Andira inermis trees varied in their relative attractiveness to bees. At one extreme, some trees attracted a wide variety of species in large numbers; at the opposite end were trees attractive to very few individuals. In between were trees attractive to large anthophorid bees such as Centris and Epicharis and to a much lesser extent to honey bees (most or all of which were Africanized); other trees were attractive to primarily honey bees and to a much less extent to large bees. Several possible explanations for differential attraction of bee taxa to A. inermis and a brief assessment of the potential impact of Africanized honey bees on native bees in our study areas are offered.
Costa Rican range horses break the hard, ripe fruits of calabah trees with their incisors and swallow the small seeds imbedded in the sugar-rich fruit pulp. The seeds survive the trip through the horse and germinate in large numbers where horses have defecated. Ripe fruits required 200kg pressure to break; fruits too hard for the horses to break required 272-553kg to break. Unbreakable fruits had thicker hulls; their presence provides an example of how a fruit trait may serve to spread seeds among more than one kind of large dispersal agent. -Author
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.
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