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Oecologia (2009) 161:221–226
DOI 10.1007/s00442-009-1372-3
123
CONCEPTS, REVIEWS AND SYNTHESES
The anomalous Kentucky coVeetree: megafaunal fruit sinking
to extinction?
David N. Zaya · Henry F. Howe
Received: 29 July 2008 / Accepted: 5 May 2009 / Published online: 2 June 2009
© Springer-Verlag 2009
Abstract The Kentucky coVeetree (Gymnocladus dioi-
cus, Fabaceae) is an ecological paradox. A rare tree in
nature in eastern and central North America, G. dioicus
produces legumes that are only known to be dispersed by
water, but appear similar to fruits consumed and dispersed
by elephants and rhinoceros. One would expect the pods to
be consumed by livestock, but the pulp and seeds are toxic
to cattle and sheep. We examine the puzzle of G. dioicus
dispersal in light of its other reproductive and life history
characteristics and Wnd that it probably is a botanical anach-
ronism, in terms of both a set of dispersal agents long
extinct and habitats, including what we term megafaunal
disclimaxes, which have disappeared. Large seeds, the
megafaunal gestault of the fruit, a dioecious mating system,
and shade-intolerance combined with vigorous cloning
suggest a widely dispersed pioneer of Miocene through
Pleistocene habitats profoundly altered by large-mammal
herbivory. As to what ate it, we can only say there were
once many candidates. We hypothesize that the plant is an
ecological anachronism, sinking to extinction in the wild.
Keywords Botanical anachronism · Megafaunal
disclimax · Gymnocladus dioicus · Megafaunal fruit
hypothesis · Seed dispersal syndromes
Introduction
The Kentucky coVeetree [Gymnocladus dioicus (L) K.
Koch, Fabaceae] is a rare, usually dioecious tree of eastern
and midwestern North America. Its range in nature extends
from southern Ontario in the north, west to Minnesota, south
to Arkansas, and north and east to New York. The species
seems to be absent from surveyor’s records in pre-settlement
Indiana (Lindsey et al. 1965), while even exhaustive cen-
suses of natural habitats in the center of its range barely
record G. dioicus (e.g., Lindsey et al. 1961). Secondary ref-
erences simply refer to it as “rare” except where planted by
people (Deam 1921). Across its entire natural range, the tree
is found in Xoodplains (Barnes et al. 1981), alongside old
locations of human habitation (Curtis 1959), and in scattered
locations in upland forests (McClain and Jackson 1980). In
nature, the species appears to be disappearing.
The only known dispersal agent of G. dioicus is water,
and that is puzzling. The legume of this tree is a large inde-
hiscent pod that contains a sweet pulp and three to seven
large seeds. Hundreds of mature pods may hang on pistil-
late trees from autumn through winter and into spring.
Seeds are brown, round, and compressed, measure 2 cm
across at the widest point, and are surrounded by a thick,
hard seed coat. Physical dormancy can be broken by scariW-
cation or soaking in concentrated acid (Baskin and Baskin
1998). The legume does not resemble the fruit of other
water-dispersed species: it is not very buoyant, contains a
sweet pulp, and is large (15–25 cm long) rather than small
and hard; seeds do not germinate underwater and sink even
after prolonged immersion (see van der Pijl 1982; Murray
1986). Despite the anomalous characteristics for a water-
dispersed species, nothing animate appears to be its primary
or secondary dispersal agent in natural and semi-natural
habitats anywhere in North America.
Communicated by John Silander.
D. N. Zaya (&) · H. F. Howe
Department of Biological Sciences (MC 066),
University of Illinois at Chicago, 845 W. Taylor Street,
Chicago, IL 60607, USA
e-mail: dzaya1@uic.edu
H. F. Howe
e-mail: hfhowe@uic.edu
222 Oecologia (2009) 161:221–226
123
The natural history of G. dioicus is inconsistent with a
large-seeded K-selected species restricted to Xoodplains.
First, the species grows well in uplands outside of its con-
temporary Xoodplain habitats, and it is considered to be
drought resistant (Huxley and GriYths 1992). Both traits
are inconsistent with Xoodplain specialization. The Xowers
appear to be adapted for generalized insect pollination, but
the species is both sparsely scattered and usually dioecious.
It is odd that an obligate outcrosser that depends on a gener-
alized insect pollination system should be rare and sparsely
scattered, as generalized pollinators are unlikely to Xy long
distances from one Xowering tree to another. On Wrst prin-
ciples, either a more eYcient pollination system that
directly delivers pollen to its targets or a greater density of
individuals should be expected (we predict that strong pol-
len limitation in G. dioicus may be common in nature
where isolated trees cannot cross with conspeciWcs,
although we are not aware of any studies addressing the
subject). In addition, G. dioicus clones vigorously in early
seral upland and Xoodplain sites (McClain and Jackson
1980) and is shade-intolerant, which in combination are
often characteristics of early-successional trees (Grime
1979). Large seed size is usually but not always an attribute
of late-successional tree; pioneer exceptions are likely tied
to particular disperser guilds (e.g., Cordeiro et al. 2004).
The Kentucky coVeetree’s contemporary ecology is a study
of contradictions.
Anachronism?
Anomalous fruits, an anomalous life history, and a dioe-
cious breeding system with generalist pollinators make it
most unlikely that this tree is “born to be rare” as a sparsely
distributed tree disseminated by water. Rather, it appears to
have the characteristics of a megafaunal fruit. Its large
heavily protected seeds, sweet pulp, and an indehiscent pod
certainly appear to put it into the “megafaunal fruit” syn-
drome, thought by Gautier-Hion et al. (1980, 1985) to be
adapted for consumption and dispersal by large mammals
(also see Alexandre 1978). Typical fruits dispersed exclu-
sively by African elephants tend to be large, with a Wbrous
pulp, indehiscent, thick-husked, brown or dull-colored, and
with seeds mechanically or perhaps chemically defended
against digestion (Gautier-Hion et al. 1985; Baskin and
Baskin 1998). This syndrome applied beyond West Africa
Wts with rhinoceros-dispersed Trewia nudiXora L. fruits in
South Asia (Dinerstein and Wemmer 1988). In the case of
G. dioicus, there are no known biotic agents (Beal 1898;
Werthner et al. 1935), leaving the paradox of a poisonous
legume that looks edible, now dispersed by water along
river courses, but thriving as rare individuals and clones in
upland sites.
An obvious hypothesis put forth by others is that the
legume of G. dioicus is a botanical anachronism; the spe-
cies was once dispersed by large mammals that are now
extinct (Janzen and Martin 1982; Barlow 2000). Janzen and
Martin (1982) elaborate this hypothesis in detail, arguing
that many tropical and temperate fruits, large and small, fall
into a megafaunal fruit syndrome of species widely and
consistently dispersed by American horses, cattle, camels,
sloths, titanotheres, and pachyderms that disappeared
before or during the Pleistocene (see Webb 1983; Janis
et al. 2004). The megafaunal fruit argument is based on the
idea that a suite of fruit attributes, including tough indehis-
cent pods and large seeds like those of G. dioicus, indicates
adaptation to megafaunal dispersal. The hypothesis is plau-
sible in light of the immense fauna of large animals—rival-
ing and even exceeding that of East Africa today—that
once roamed North America (Kurtén and Anderson 1980;
TiVney 2004). At the same time, the pod contains a thick
pulp that is sweet but poisonous to humans and livestock
(Tehon et al. 1946; Kingsbury 1964; Evers and Link 1972).
Apparent toxicity to contemporary ungulates sets the
legume apart from other megafaunal fruits, which are often
avidly consumed by domestic livestock that Janzen and
Martin (1982) plausibly view as surrogate megafaunal dis-
persal agents. Cattle and other livestock are not surrogate
dispersal agents of this tree.
We agree that G. dioicus belongs in the megafaunal syn-
drome, despite paradoxical attributes of this tree and ambi-
guities in the syndrome itself (Howe 1985). Although there
is a virtual absence of primary literature on the ecology of
this rare and apparently vanishing species in nature (i.e.,
we know of two papers in the last 50 years: Janzen 1976;
McClain and Jackson 1980), we Wnd enough evidence in
secondary and tangential resources to have conWdence that
the tree has an interesting story that should be told. Accord-
ingly, we extend the megafaunal syndrome to include
corroborating evidence from its life history and mating
system, discuss characteristics of G. dioicus that could help
it survive without its primary dispersers, and puzzle about
the toxic anomaly.
The established syndrome
“A dispersal syndrome is a constellation of fruit and seed
characteristics which is associated with a general mode of
dispersal” (van der Pijl 1982). Dispersal syndromes deWne
trends, but they are of less use in predicting particular dis-
persal interactions (Howe and Smallwood 1982; Howe
1985; Herrera 2002). In the case of G. dioicus, the question
is not what eats the fruit, but whether anything ever ate the
fruit. It is easier to distinguish between abiotic and biotic
dispersal than between diVerent biotic agents. The strong
Oecologia (2009) 161:221–226 223
123
resemblance to general characteristics of megafaunal fruits
and its deviation from usual characteristics of water-
dispersed species suggests that this legume is adapted to be
consumed. Fruit size is well correlated with disperser size
(Jordano 1995), and seeds as large as those of G. dioicus
are almost always dispersed by large vertebrates (Hughes
et al. 1994) or large rodents. In this case, both are either
absent or do not eat or hoard the seeds where the tree
occurs.
The key characteristics used by Janzen and Martin
(1982) to deWne a megafaunal fruit syndrome include: (1) a
large and indehiscent structure; (2) pulp that is rich in
sugar, oil, or nitrogen; (3) similarity to Old World fruits
currently dispersed by extant megafauna; (4) nuts and seeds
that are well protected mechanically to prevent damage by
the teeth of megafauna; (5) fruits attract few or no extant
native vertebrates; (6) undispersed seed crops that rot on
the ground beneath fruiting trees; (7) fruits that are avidly
consumed by horses, pigs, and cattle, which act as replace-
ments for the extinct megafauna. The hypothesis is emi-
nently plausible, although Howe (1985) noted that species
ascribed to the syndrome would have to experience low
seedling mortality near the parent tree to persist and that
some fruits listed as examples had known extant dispersal
agents. The syndrome has since been quantitatively
described by Guimaraes et al. (2008), who distinguish
large-seeded species, such as G. dioicus, from other com-
pound fruits with many small seeds. In any event, G. dioicus
Wts the Janzen and Martin criteria almost perfectly, except
that the legume and seed are toxic to livestock. For this to
be a megafaunal fruit, the extinct megafauna would have to
have included taxa that could consume toxins not metabo-
lized by livestock alive today.
It is not obvious what the active mammalian toxin in
G. dioicus might be. Early evaluations noted the alkaloid
cytosine, which has similar bonding properties as nicotine
but which is not as potent for humans (for an ecological
interpretation, see Janzen 1976). More recent evaluations
have found triterpenoid saponins in an Asian congener that
are biologically active enough to be potential anti-human
immunodeWciency viral (HIV) agents (Konoshima et al.
1995). Gymnocladus dioicus itself has nonprotein amino
acids (Oh et al. 1995), which can be extraordinarily potent
allelochemical defenses for most herbivores (Rosenthal
1991). However, the collection of nonprotein amino acids
found in G. dioicus is similar to that found in another North
American legume, Gleditsia tricanthos L. (Southon et al.
1994), which has legumes that are not poisonous to humans
and are readily consumed by livestock (Evans and Bell
1978). Glycosides of terpenoid derivatives isolated from
G. dioicus are also suspected of being sources of toxicity
(Burrows and Tyrl 2001). There is no direct evidence that
these are the active compounds that deter contemporary
mammals, much less active toxins or their synergies once
overcome by extinct megaherbivores. Given the reality of
multiple defenses in many trees and the absence of relevant
surrogates in the modern fauna of North America, the roles
of allelochemicals will probably remain a mystery without
a massive, and unlikely, titration of livestock responses to
chemical and structural components of the plant.
Persistence
The loss of megafaunal dispersers can be catastrophic to
dependent tree populations, leading to rapid decline and
extirpation (Alexandre 1978; Dinerstein and Wemmer
1988; Cochrane 2003). How could G. dioicus survive for so
long? The persistence of G. dioicus—or any species—after
13,000 years without its primary dispersers begs for expla-
nation. We argue that traits which allow for resilience are
an important part of a reWned megafaunal fruit syndrome.
Several characteristics of G. dioicus increase the odds that
it could persist for millennia without its primary dispersers
(Barlow 2000). As an ornamental, the foliage and, more
importantly, the seeds of G. dioicus are aZicted by very
few pathogens (Pirone 1978) and are free from almost all
herbivores and seed predators (Werthner et al. 1935; Pan
et al. 1995). Moreover, its seeds resist decay for years
(DNZ, personal observation) and are protected by an
exceedingly hard seed coat. This Wts the criterion of “inde-
structible oVspring” (Howe 1985, 1989) required for persis-
tence for millennia without megafaunal dispersers. The
absence of seed predators is important because a plant with
high seedling mortality near the parent tree would not sur-
vive for thousands of years without some agent dispersing
its seeds eVectively. Species with seeds that are dispersed in
clumps, such as in fecal piles of large fruit-eating dispersal
agents, should be more likely to develop adaptations for
protection against pathogens and seed predators and thus
should be more likely to persist without primary dispersers.
In studies on suspected anachronistic fruits in Brazil,
Guimaraes et al. (2008) found that many species were able
to persist because of the water dispersal of seeds, asexual
reproduction, and Native American use. All three of these
factors are probably important in the survival of G. dioicus.
As mentioned earlier, seeds are now water-dispersed
despite poor Xotation. Additionally, G. dioicus is able to
multiply asexually through basal sprouts extending from
the root system (McClain and Jackson 1980), and stands of
G. dioicus often occur near abandoned human habitations
(often along rivers) where Native Americans and early
European pioneers used seeds for game pieces and as a sub-
stitute for coVee (Curtis 1959; e.g., stands of trees on ridge-
tops near 1000-year-old burial mounds at EYgy Mounds
National Monument, Iowa; HFH, personal observation).
224 Oecologia (2009) 161:221–226
123
The tree is not physiologically dependent on Xoodplains.
Indeed, the comprehensive autecology of the tree by
McClain and Jackson (1980) suggests that many Xoodplain
sites probably correspond to former Native American
settlements. Even Xoodplain presence may be an agency of
something besides water.
What is missing?
Gymnocladus dioicus is hypothesized to have arrived in
North America in the Miocene (TiVney and Manchester
2001), coincident with the explosive adaptive radiation of
large mammalian herbivores on the continent (Wing and
TiVney 1987; Janis 1993; Alroy 1999; TiVney 2004). Dur-
ing the Miocene, 25–5 mybp, mammalian herbivores capa-
ble of dispersing Gymnocladus could have included North
American rhinos, camels, or small- to medium-sized gomp-
hotheres (Webb 1983; Janis et al. 2004). Modern livestock
would have been dwarfed in diversity and size by many
Miocene mammals, and thus are not necessarily good sur-
rogates for extinct megafaunal dispersal agents.
Could some of the large herbivores have eaten the fruit
and its toxins without ordeal, and be the primary dispersal
agents? No one knows, but the Miocene had numerous can-
didates. A particular genus or species might have evolved a
capacity to detoxify the active agent. The more likely sce-
nario is that the capacity for feeding on toxic plant com-
pounds increases with body size because the number,
diversity, and volume of bacteria and protozoan symbionts
that detoxify plant defenses increase with body size
(Farlow 1987; Van Soest 1994; Fritz et al. 2002), suggest-
ing that extinct megafauna substantially larger than con-
temporary sheep (30 kg) or large cattle (250 kg) could have
consumed the legume of G. dioicus and been responsible
for its dispersal. This hypothesis is entirely consistent with
TiVney’s (2004) interpretation that megafaunal dispersal is
a diVuse process. Elephants (Loxodonta africana Blumen-
bach) readily eat and disperse some fruits that are not eaten
by other animals (Gautier-Hion et al. 1985; Dudley 2000),
and black rhinoceros in southern Africa often consume the
fruits and stems of highly toxic Euphorbia species that are
avoided by other animals (Heilmann et al. 2006; see Kinghorn
1979). A variety of large non-elephantine mammals may
have had similar capacities, followed by mastodont- and
mammoth-sized herbivores. Extinct North American
ground sloths (Nothrotheriops shastensis HoVstetter), for
instance, did not leave fruits like G. dioicus in coprolites,
and in general seemed to feed on fairly digestible forage,
but they did eat some plants (Ephedra, Gueterrizia, Larrea)
that livestock—and just about everything else—now avoid
(Hansen 1978; Hofreiter et al. 2000). It is quite possible
that the body size and enhanced gut volume of very large
mammals of the pre-Pleistocene and Pleistocene made
G. dioicus legumes a regular food for megaherbivores that
“mesoherbivores” like horses and cattle cannot eat. The
toxicity of the legume and seeds may have served as
protection from seed predators and ineVective dispersers
(Cipolinni and Levey 1997). In keeping with the consensus
that interaction of a fruiting plant is usually with a group of
functionally equivalent dispersal agents rather than a single
species (Janzen 1980; Howe 1984; Herrera 1985; Wing
and TiVney 1987; TiVney 2004), diVuse dispersal between
G. dioicus and a set of large mammalian dispersal agents is
likely part of what is missing.
In addition to missing dispersal agents, the habitats to
which G. dioicus is well-suited almost certainly no longer
exist in North America. African trees that survive in habi-
tats frequented by elephants are likely to be highly toxic
(Sheil and Salim 2004). The same may have been true of
now extinct North American habitats once frequented and
probably shaped by extinct mastodonts, mammoths, less
familiar gomphotheres, rhinos, and camels of the Miocene
or early and middle Pleistocene. Reconstructions of Xora
tens of thousands of years ago paint only in a broad brush,
but show ample evidence of massive changes in climate
and vegetation during the tenure of G. dioicus in North
America (see Webb 1983). More detailed reconstructions
of Pleistocene habitats from much more complete fossil
records leave little doubt that contemporary grasslands,
savannas, and forests are incomplete reXections of the
much more diverse associations of animals and plants that
existed even 500,000–10,000 years ago (Guthrie 1984;
Davis 1986; Overpeck et al. 1992; Graham et al. 1996;
Jackson et al. 2000). As recently as 12,000 years ago, most
of Central North America, probably coinciding with most
of the range of G. dioicus, was covered with forests of com-
positions with no modern analogs (Overpeck et al. 1992).
The contrast between contemporary environments in which
G. dioicus barely persists in the wild and a much richer
diversity of habitats of the recent to distant past leads us to
speculate what world the tree might have found suitable.
Megafaunal disclimaxes
We hypothesize that the entire life cycle of G. dioicus is a
relict of processes and environments driven by large mam-
mals, long gone. Owen-Smith (1987) points out that Afri-
can megaherbivores, such as elephants and giraVes, are so
large that they are invulnerable to signiWcant non-human
predation. Unless disease intervenes, they saturate their
habitats, causing so much destruction that forest is con-
verted to scrub and grassland. We suggest that these highly
disturbed habitats, what we term “megafaunal discli-
maxes,” were the cradle for the evolution and proliferation
Oecologia (2009) 161:221–226 225
123
of species adapted to megafaunal dispersal. One could
imagine population cycles of North American megaherbi-
vores, sometimes decimated by disease and at other times
released to their destructive potential, that created perma-
nent transitional plant dynamics. With their world in a per-
manent state of successional Xux, even modest dispersal
rates of large seeds of a species that grows anywhere in a
disturbed habitat, clones freely, is shade-intolerant, resists
insects and pathogens, and is distasteful or toxic to most
mammals might be a winning megafaunal tree. Such trees
might grow in poorly dispersed clumps where dioecy is not
a disadvantage, with occasional or even frequent dispersal
by very large mammals that could eat a few fruits without
ill eVects. Such a tree might have been Gymnocladus
dioicus.
Acknowledgments We thank Usama Ahmad, Luca Borghesio,
Crystal Guzman, Maria Luisa Jorge, William Lu, Jennifer Ison, Andrea
Kramer, Gabriela Nunez-Iturri, Manette Sandor, Carrie Seltzer, John
Silander, Amy Sullivan, Bruce TiVney, Mariana Valencia, Jenny Zam-
brano, and anonymous reviewers for comments on the manuscript. We
gratefully acknowledge support from the Archbold Biological Station,
the University of Illinois at Chicago, and the National Science Founda-
tion (DEB 0129081, 0516259). Procedures conformed to federal, state
and local laws and permit regulations.
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