Walking on campus last month I spotted an acquaintance I had long overlooked—a Kentucky Coffee tree, Gymnocladus dioicus. It’s small and easy to miss most of the year, but one characteristic stood out—the ear-sized seedpods that had clung to its branches well into the  Spring. Early American caffeine addicts ground up its large seeds to make a coffee substitute. If they got a buzz it wasn’t from caffeine–a novel amino acid makes up 5% of the seed contents (dry weight), probably toxic to the Bruchid beetles that plague most other Leguminosae (Janzen, 1969), but a welcome winter snack  for a hungry mastodon or ground sloth. G. dioicus shows all indications of being an ice age orphan–left hanging by its normal dispersers (Barlow, 2000). Native Americans may have saved the tree from extinction by spreading the seeds for food or perhaps to use for recreation  (Van der Linden and Farrar, 1984). (tree photo borrowed from)

Janzen and Martin (1982) cite large wasting fruit and seeds as indications a plant may be a victim of the ice age extinctions. On that basis the Honey Locust, Osage Orange, Persimmon and Pawpaw are most often cited as other orphans (Barlow, 2000). I wonder though if this list doesn’t significantly understate the impact of the mass-extinction on plants. “Large” and “wasting” are nebulous measures, and little is  known for sure about the fate of seeds after they leave home. (seed photo borrowed from)

However transported, and some compelling models not withstanding, few researchers have ever had the wherewithal to track an actual seed shadow. Forgotten rotting fruit may be the least of the waste. An oak, for example,  need only see one acorn mature among the millions it produces over a lifetime to be deemed a success. The thousands eaten by squirrels and blue jays annually may be the necessary “payment in offspring” owed to dispersers for their service (Janzen, 1985), but the 90%+  lost annually to pathogens, insects and seed predators (Janzen, 1969), or simply misplaced, is a huge waste! (oak photo by Richard Packwood,  borrowed from)

Evolution is a sloppy business, and forces of selection assail a plant from all directions. Fruit characteristics are a compromise between defense and attraction.  Perfectly choreographed plant-disperser relationships are rare, and what passes for the dance of coevolution is usually just an animal doing an opportune solo and “fitting” in (Janzen, 1969) using a suite of morphological features and behaviors evolved eons earlier in a different habitat, and in the case of sloths, a different continent.  For G. dioicus, Megalonyx was simply “next” in a long line of big movers, possibly stretching back to dinosaurs.

Plants generally don’t do much adapting to the dispersers they are dealt. Like in high school, there’s strong pressure from the surrounding community to look and act like everyone else–in this case a fruit.  Invasive species wouldn’t be the problem they are if evolution put a premium on dispersee individuality.   Fossils show the basic characteristics of many fruits have persisted over very long periods of time. The arils of Taxus, for example, are virtually indistinguishable today from those of Palaeotaxus 175 million years ago (Herrera, 1986). Flowering plant species show up in the fossil record an average of 27-38 million years, while birds and mammals last for just 0.5-4.0 million years (Herrera, 1985a). Disappearing dispersers, i.e. orphaning, is a recurring event in the evolutionary lives of plants. “Smart” trees don’t put all their eggs in one basket and coevolve with just a single disperser unless they run out of options, as on an island. (Taxus photo borrowed from)

Like “waste,” size is relative too, and a poor measure of disperser compatibility. I’ve always been struck by the dependence of Yellowstone grizzly bears on White-bark Pine seeds (Pinus alibicaulis) (Kendall, 1983). Howsoever small, pine nuts pack a wallop of nutrition, offsetting the bears’ high handling costs.   Grizzlies eat various small fruit throughout their range, and travel some distance to get it (Willson, 1993). Size isn’t a constraint so long as a fruit returns the investment. (Bear photo borrowed from)

The individual fruits of many woody plants are small and seem adapted for the exclusive dispersal of birds and small mammals, but they often grow in compact bundles of multiple “berries.”  Frequently the bundles or infructescences are located on the ends of branches. This presentation may have evolved to compete better for the attention of passing birds, or to swamp insect pests (Sallabanks and Courtney, 1992); it may make the fruit harder for small rodents to steal (Denslow and Moermond, 1982), or enhance pollination chances (Schoen and Dubec, 1990); it may just be the most efficient structure for the plant (ibid.), but it also certainly reduces the handling costs of large mammals. No need to seach far and wide for large fruit when plenty of prepackaged small fruit is readily available.

There’s little allure however in an infructescence whose individual berries don’t ripen simultaneously, forcing foragers to waste time picking over bundles looking for ripe fruit.  Not coincidentally, synchronous ripening is characteristic of most of North America’s fruiting plants, especially in the fall when demand is greatest (Thompson and Willson, 1979).  Bundling easily accessible mouthfuls of fruit is a wise risk-hedge for a plant living in an uncertain world where dispersers both big and small drop out regularly.

Given the opportunity, many mammals include fruit in their diets, and most that do are legitimate dispersers on occasion (Sallabanks and Courtney, 1992).  So does it matter that North America’s small-fruited trees and shrubs lost their largest potential dispersers 12,000 years ago?  . . . There are still plenty of birds around.  Are plants suffering for lack of super-sized transport service?  Is there any reason to believe Megalonyx played any significant role in the process?

Fleshy fruit and dedicated fruit-eaters are relatively uncommon in North America today compared to the diversity of the neotropics (Howe, 1986).  Explanations usually include the constraints of winter and the plants’ habitat requirements.  Many are fugitive species, dependent on forest edges and clearings, a tree-fall or fire to open a gap for them to become established, and declining when the late-successioners reassert their dominance (Herrera, 1985b).  However, our deficit may simply be the fallout from an impoverished forest disturbance regime crippled by the extinction of the ice age megaherbivores.  (elephant photo borrowed from)

“It matters who defecates what where” (Janzen, 1986), most particularly because of what else they are doing at the time.    Whether Megalonyx served as a disperser or not, the  megaherbivores played keystone roles in the disturbance regime of Ice Age woodlands, creating the openings  fruiting plants need in particular.  If the surviving fruiting species aren’t dispersal orphans, many are certainly disturbance orphans. . . . Dave

References

Barlow, C. 2000. The Ghosts of Evolution: Nonsensical fruit, missing partners, and other ecological anachronisms. Basic Books. New York, NY.

Denslow, J. S. and Moermond, T. C. 1982.  The effect of accessibility on rates of fruit removal from tropical shrubs:  an experimental study. Oecologia 54: 170-176.

Herrera, C. M. 1985a. Determinants of plant-animal coevolution: the case of mutualistic dispersal of seeds by vertebrates. Oikos 44: 132-141.

Herrera, C. M. 1985b. Habitat-consumer interactions in frugivorous birds.  In Habitat Selection in Birds.  M. L. Cody (ed.).  Academic Press,  Orlando, FL.

Herrera, C. M. 1986. Vertebrate dispersed plants: why they don’t behave the way they should. In Frugivores and Seed Dispersal. A. Estada and T. H. Fleming (eds.). Dr. W. Junk Publishers, Dordrecht.

Howe, H. F. 1986.  Seed dispersal by fruit-eating birds and mammals.  In Seed Dispersal.  D. R. Murray (ed.). Academic Press, NY.

Janzen, D. H. 1969.  Seed-eaters versus seed size, number, toxicity and dispersal.  Evolution 23: 1-27.

Janzen, D. H. 1985.  The natural history of mutualisms.  In The Biology of Mutualism:  Ecology and Evolution.  D. H. Boucher (ed.) Croom Helm Ltd., London.

Janzen, D. H. 1986.  Mice, big mammals, and seeds:  it matters who defecates what where.  In Frugivores and Seed Dispersal.  A. Estrada and T. H. Fleming (eds.) Dr W. Junk, Publishers, Dordrecht.

Janzen, D. H. and Martin, P. S. 1982. Neotropical anachronisms: the fruits the Gomphotheres ate. Science 215: 19-27.

Kendall, K. C. 1983. Use of pine nuts by grizzly and black bears in the Yellowstone area. International Conference on Bear Research and Management 5: 166-173.

Sallabanks, R. and Courtney, S. P. 1992.  Frugivory, seed predation, and insect-vertebrate interactions.  Annual Review of Entomology 37: 377-400.

Schoen, D. J. and Dubec, M. 1990.  The evolution of inflorescence size and number: a gamete-packaging strategy in plants.  The American Naturalist 135: 841-857.

Thompson, J. N. and Willson, M. F. 1979. Evolution of temperate fruit/bird interactions: phenological strategies.  Evolution 33: 973-982. 

Vander Linden, P. and Farrar, D. 1984. Forest and Shade Trees of Iowa. Iowa State University Press. Ames, IA.

Willson, M. F. 1993. Mammals as seed dipersal mutualists in North America.  Oikos 67: 159-176.

UNC Charlotte Botanical Gardens

The city of Marion is soliciting ideas from local residents and other interested parties for improving city life and strengthening its identity in a program they are calling Imagine8.  I’ve been working with a group of friends and supporters of the Eastern Iowa Paleontology Project (EIPP) to develop a statement encouraging an initiative to improve natural science education in the city.  We all agree it would be very nice if we can create a permanent home for our dinosaur in the process, but more important is encouraging science education.  You would think with the shortage of engineers, scientists, doctors and other health professionals in this country and our pressing environmental needs that there would be more support for teachers and families wanting to encourage their children in this direction but science funding always trails far behind that for culture and the arts.   Since Cedar Rapids hasn’t called me yet about redeveloping their flooded downtown area into an Ice Age Sloth Park ,  I’m planning  to dust off the idea for Marion and propose it as part of a general botanical center.

Proposed:  To promote natural science education and build a strong community identity Marion should establish a botanical center managed like the Chicago Botanic Garden and the Minnesota Landscape Arboretum in Minnneapolis (among many others).  A huge volunteer army has formed to help maintain these gardens and they have become the center of social activity in their communities.  E. Iowa garden clubs are as varied as the plant world, with different ones devoted to roses, hostas, water plants, fruit, vegetables,  herbs, heirloom plants, prairies, succulents, conifers, terrariums and bonsai, in addition to several with a general interest.  Every one would volunteer to design, plant and maintain a garden focused on their passion, and where no club currently exists one would quickly coalesce from local experts given the opportunity.  

A botanical center would be a distinctive jewel for Marion and a magnet for senior citizens, school teachers, tourists and families interested in nature, birding, wildlife, ecology, etc.   A botanic garden would send a powerful signal to business about the community’s commitment to children and science education. The center would become an important nexus between area colleges and universities, with Kirkwood (the local community college) offering considerable practical horticultural experience and students; Iowa State University (in nearby Ames) adding a high-tech/ag/research dimension; and the University of Iowa  bringing an impressive collection of paleobotanical fossils and expertise to the table, in addition to a world-famous environmental engineering program. 

Partnerships might also be explored with the many area companies involved in the agriculture, bioremediation and biofuel industries. With a small staff committed to coordinating self-governing volunteer organizations, and the research operations funded by industry and the universities, operating costs would stay low versus the benefits reaped.  Gardeners are patient, with nurturing as the objective, not immediate gratification, so unlike any other project the city will consider, a botanical center would pay dividends from its inception, expand as the budget and Marion’s vision permits, and improve with age.

That’s my proposal.  A Sloth Woodland and a Dinosaur Fern Garden would be terrific family attractions in a botanical center.  If you want to submit some ideas of your own supporting paleontology, natural science, or children’s science education here’s a link to the Marion Imagine8 home page. . . . Dave. 

We’re like Goldilocks wandering around in the cottage of The 3 Sloths—the table is set, the beds are made and the TV is on—maybe the owners are out in back . . . but we’re pretending they’re gone forever and we’re in control now. Look around—sloths may be extinct, but they aren’t dead! We’re surrounded by signs of their lingering presence, and the continuing performance of many of their Ice Age co-stars. Applaud Blue Jays today for our oak trees. Admire the Osage Orange that still grows a formidable sloth defense. And grieve for the lonely Honeylocust that still cries out every fall for the sloths to return. (photo borrowed from)

The common Honeylocust (Gleditsia triacanthos), sometimes called the “False Acacia,” is reviled despite many fine qualities including light shade, fragrant flowers and adaptability. The problem? #1: its large thorns—a serious menace to tires and bare feet, and; #2: the messy piles of long curly brown seedpods produced by the females. (photo borrowed from)

The “honey” in “honeylocust” comes from the sweet gum that surrounds the seeds while they ripen inside the pods. “Locust” is a case of mistaken identity. Colonial settlers assumed G. triacanthos was related to the Old World Carob or Locust (Ceratonia siliqua), a Mediterranean tree with similar pods (Peattie, 1991). A chocolate substitute is ground from the seeds. The tree’s nickname, “St.-John’s Bread, ” is a biblical reference to the sweet-toothed saint who subsisted on ”locusts and wild honey“ in the desert (Matthew 3:4). Scholars believe he was eating Ceratonia seeds rather than bugs and the “locust” derives from the resemblance of the noisy insects to the rattling sound the pods make when ripe and the tree branches are shaken (Peattie, 1991). (photo borrowed from)

G. triacanthos is an aggressive colonizer of disturbed ground (e.g. farm fencerows, ravines and abandoned pastures; floodplains); once established they are hard to eradicate (Illinois Nature Preserves Commission, 2003). Saplings display imposing ever-growing clusters of thorns, some over 12 inches long (The Complete Encyclopedia of Trees and Shrubs, 2003). The multi-branched spikes can cover the trunk to a height of 20+ ft.– far beyond the reach of living browsers. Defensive overkill is good sign of an ice age ghost at work and the lingering effect of genes that know mastodons and sloths are still lurking nearby (Barlow, 2000). (photo borrowed from)

G. triacanthos is an ice age orphan–seedpods don’t pile up like they do under this tree unless its regular disperser(s) are gone (Janzen and Martin, 1982). An “aggressive colonizer” doesn’t sound like it’s suffering, but the trees’ common occurrence along river bottoms is an important clue—spring floods carry the seedpods afar but there are problems moving upstream and to high ground. For most of the Holocene, with its natural dispersers extinct, G. triacanthos was rare within its former range (Janzen 1982). It only became widely distributed again after cattle were introduced to North America. The prowess cows show in dispersing Honeylocust seeds results from evolving with very similar trees, Acacia spp., in N. Africa and the Middle East. Looking at Acacias and the relationships they co-evolved with large ungulates may reveal some important clues about Ice Age ecosystems and also sloths. (photo borrowed from)

There are 128 Acacia spp. in Africa; nearly half concentrated in the Horn of Africa and the Middle East (Coe and Coe, 1987). All mount a defense of hooks or spines against browsers; some famously offer bed and board to stinging ants for reinforcement. Acacia foliage is valuable forage for herbivores throughout Africa, and in the dry season the bark is an important item in elephants’ diets. The seedpods are avidly eaten by many large ungulates. Some pods contain a sticky aromatic secretion that is it is eagerly sought by browsers. (photo borrowed from)

Some Acacia seeds are small and papery and wind-dispersed; others are large and durable and dispersed by mammals. Traditional pastoralists harvest the latter to feed livestock, using long poles to shake the pods down from the trees. The seeds rattle inside the pods and the sound attracts animals from up to 200 meters away (Coe and Coe, 1987). Mutualistic relationships have developed from the Sahara to India between arboreal mammals feeding in Acacia trees and land-bound browsers attracted to the sound and dropped pods.

Acacia seeds won’t germinate in the shade of their parents so wind or good wheels are important for dispersal (Miller and Coe, 1993). The hard seeds are well adapted to survive the shearing forces of mammal teeth and digestive acids. They need scarification to speed germination, and the more the better. Rohner and Ward (1999) found a significant correlation between mammal size and germination success. However, the same architecture that allows the seeds to escape mammal-passage largely unscathed also leaves them vulnerable to Bruchid beetles, or “seed weevils.” The insects bore through the Acacia pods while they are still green and growing on the trees and lay their eggs on the seeds. The new generation attacks the mature seeds and can destroy up to 99% of those left on or under the trees (Southgate, 1981). (photo borrowed from)

With death by beetle infestation virtually certain, could a seed be any worse off getting eaten? Surprisingly, those seeds that go through a mammal gut have a germination rate up to 3X better than seeds that aren’t swallowed (Miller and Coe, 1993). If caught early, ingestion kills the Bruchid larvae before they kill the seed, and the tunnel the insects burrowed inside speeds water absorption and germination later on. It’s extremely beneficial for Acacias to arrange to have their seeds eaten as soon as possible after ripening, and transported far away from the site of infestation, so they evolved a dinner bell. When ripe. they start rattling, like a Flamenco dancer on caffeine, and mammals come running from all around.  And so too it worked for the Honeylocust for millennia. . . . (photo borrowed from)

Ecologists have barely begun to decipher the many ways ice age megamammals affected North American ecosystems. Species may be orphaned in many ways–the signs are often subtle, like the call to dinner that no one hears. As we survey the woodlands we’ve inherited we should remember that the sloths haven’t been gone as long as we pretend—the porridge is still hot and their music still plays. And as the quickening pace of global climate change and related “natural” disasters indicate, we aren’t in control at all. We’ll never solve some of our conservation puzzles until we acknowledge the keystone role of the Pleistocene megamammals (photo borrowed from). . . . Dave

References:

Barlow, C. 2000. The Ghosts of Evolution: Nonsensical fruit, missing partners, and other ecological anachronisms. Basic Books. New York, NY.

Coe, M. and Coe, C. 1987. Large herbivores, acacia trees and bruchid beetles. South African Journal of Science 83: 624-635.

Dirr, M.A. 1997. Dirr’s Hardy Trees and Shrubs, Timber Press, Portland, OR.

Etherington, K. and Imwold, D. (eds.) 2003. The Complete Encyclopedia of Trees and Shrubs. 2003. Thunder Bay Press. San Diego CA.

Illinois Nature Preserves Commission. 2003. Vegetation Management Guideline: Honey Locust (Gleditsia triacanthos L.).  Vol. 1, No. 30.

Janzen, D.H. 1982. Fruits for famished mammoths. Garden 6: 12-24, 32.

Janzen, D.H.and Martin, P.S. 1982. Neotropical anachronisms: the fruits the gomphotheres ate. Science 215: 19-27.

Miller, M.F. and Coe, M. 1993. Is it advantageous for Acacia seeds to be eaten by Ungulates? Oikos 66: 364-368

Peattie, D.C. 1991. Natural History of Trees of Eastern and Central North America. Houghton Mifflin Company, Boston, MA

Rohner, C. and Ward, D. 1999. Large mammalian herbivores and conservation of arid Acacia stands in the Middle East. Conservation Biology 13: 1162-1171.

Southgate, B.J. 1981. Univoltine and multivoltine cycles: their significance. In The Ecology of Bruchids Attacking Legumes (Pulses). Junk, The Hague. pp.17-22.

Fussy birds get what they deserve—that’s how some ornithologists explain the demise of birds like the Ivory-billed Woodpecker (Campephillus principalis) (Shugart, 2004). Ivory-bills foraged for insects by prying up the bark of large trees, leaving it to other woodpeckers to probe the deeper reaches.  There’s a limited supply of suitably-clad trees so the birds needed large territories—at least 36 miles² by one account (ibid.). Under this scenario agricultural land-clearing and hunting were just the final nails-in-the-coffin.  One might be skeptical of explanations of extinction that blame the victim for choosing an unreliable niche.  Trees die for many reasons–senescence, lightning, disease, over-browsing, floods, droughts, ice, wind-throw . . . all contributing to the dynamic patchwork that characterizes a healthy diverse woodland.  The birds wouldn’t have evolved their habits if they didn’t have a reliable food-supply for millions of years and the behavioral elasticity to take advantage of the opportunities that arose and overcome challenges.  Something significant altered the woodland disturbance regime.  In that gap, and missing from the list above may reside an ice age ghost–keystone mega-herbivores that played a critical role in ancient forests–as the giants do today wherever they have survived (Owen-Smith, 1987). (picky eater photo borrowed from, woodpecker photo borrowed from)

Central American trees with piles of wasted fruit first drew the attention of Janzen and Martin (1982).  They suggested the dispersers with whom the plants had evolved had become extinct at the end of the Pleistocene and coined the term Ice Age “orphans” to describe the plants.  Barlow (2000) identified mammoths, mastodons, ground sloths and other extinct mammals as the “ghosts” of the Ice Age that explained the surplus fruit and  extravagant defenses of certain plants and animals (Byers, 1997).

C. principalis may be another Ice Age orphan.  African elephants are notorious for rubbing, girdling, debarking and toppling trees (Coe and Coe, 1987). For millions of years Ivory-bills probably enjoyed a steady supply of dead and dying trees courtesy of mastodons, ground sloths, etc. .  Habitat loss to humans and hunting may have just sealed their fate—perhaps they were doomed 12,000 years ago with the extinction of their keystone partners. 

There is much natural history work that merits reexamination with Ice Age ghosts in mind. Hints of “missing links” abound in the accounts of extinct and endangered birds, for example, in the uncertainty about the extinction of the Carolina Parakeet (Conuropsis carolinensis). The parrots became scarce before the peak of plumage-hunting.  They were said to be the bane of fruit-growers and may have been shot as pests, but McKinley (1960) notes the birds never earned a place on any bounty lists.  He suggests honeybees were their undoing.  Introduced by early European settlers, the bees competed with the parakeets for the tree-hollows they needed for nesting and roosting.   As with the Ivory-bill, the lack of suitable tree habitat suggests a crimp in the supply chain–a disruption in the natural disturbance regime.  Snags and the dead wood on living trees provide important habitat for 25% of the species that live in eastern forests today (Pennsylvania Game Commission, 2008).  It’s vital to learn the right ecological lessons if we are to remediate the threat facing today’s woodland residents.  (photo borrowed from)

An erratic food supply, pesticides and lead poisoning are the oft-cited reasons for the near-extinction of the California Condor, Gymnogyps californianus, but Cowles (1967) suggests as western scrubland became overgrown with brush, condors were blocked from exploiting key habitat and food sources. The birds need a stiff breeze and a running start to overcome the weight of a meal and fly (USDA Forest Service, Index of Species, 2008).  With their runways blocked by high vegetation the birds remain airborne today over vast portions of their former range.   Cowles points to fire suppression for the brush buildup, but the real cause may be the extinction of the browsers that once kept the vegetation down e.g. mastodons, camels (Camelops spp.), Harrington’s mountain goat (Oreamnos harringtoni) and the Shasta Sloth  (Nothrotheriops shastensis). It may be no coincidence that the Condor disappeared from the Grand Canyon at about the same time the mega-browsers became extinct (Emslie (1987).  (photo borrowed from)

Lack of mega-carrion is often blamed for the extinction of the incredible Teratornis spp.  and the other great Ice Age condors (Wetmore, 1956), but hints from Africa point to more ghosts.  Condors need large amounts of calcium in the breeding season for their eggs and nestlings.   Meat contains very little—11 mg per 100 g (Mundy and Ledger, 1976).  Calcium shortage has been linked to the small clutch size of G. californianus–one egg usually—and the very slow growth rate of their chicks (Snyder and Snyder, 2000), plus the aforementioned lead poisoning (Pb²⁺ readily supplants Ca²⁺ in their eggshells and bones). Condors normally get their calcium by swallowing the bones of small animals or the chips of bone left by scavengers at larger carcasses–the birds can’t break large bones. Mundy and Ledger (1976) link the endangered status of the Cape Griffon Vulture (Gyps coprotheres) to the extirpation of bone-crushing scavengers, especially hyenas, over broad areas of S. Africa. 20% of the bone fragments they collected at the nests of Whitebacked Vultures (Gyps africanus) in Zimbabwe, where the carnivores are extant, showed visible carnivore tooth-damage. Without sufficient calcium the bones of the Griffon chicks are deformed and break under stress like simple pre-flight exercise; often they are malnourished, their digestive tracts clogged with the detritus they ingest seeking calcium (e.g. ceramic fragments, stones, etc.) (ibid).  The extinction of the American hyena (Chasmaporthetes ossifragus) and other carnivores may have precipitated a similar calcium-crisis in North American condors. (photo by Alistair Robertson)

Ecologists have long focused on human activity and the historic forces affecting the fate of wildlife, overlooking the echoing effects of the ice ages. If we are to preserve the vanishing remnants of the natural world it’s imperative that we understand the essential forces once supplied by the Pleistocene mega-mammals and arrange for substitutes where possible, or create them ourselves by artificial means. . . . Dave

References

C

Snyder, N.F.R. and Snyder, H.A 2000.  The California Condor:  a saga of natural history and conservation.

Cowles, R.B. 1967. Fire suppression, faunal changes and condor diets.  Tall Timber Fire Ecology Conference 7: 217-224.

Emslie, S.D. 1987.  Age and diet of fossil California Condor in Grand Canyon, Arizona. Science 237: 768-770. 

Janzen, D.H. and Martin, P.S. 1982.   Neotropical anachronisms:  the fruits the Gomphotheres ate.  Science 215: 19-27.

McKinley, D. 1960. The Carolina Parakeet in pioneer Missouri.  The Wilson Bulletin 72: 274-287.

Mundy, P.J.  and Ledger, J.A. 1976. Griffon Vultures, carnivores and bones.  South African Journal of Science 72: 106-110.

Owen-Smith, R.N. 1987. Pleistocene extinctions:  the pivotal role of megaherbivores.  Paleobiology 13: 351-362.

Pennsylvania Game Commission. 2008.

Shugart, H. H.  2004. How the Earthquake Bird Got Its Name and Other Tales of an Unbalanced Nature.  Yale University Press New Haven, CT

USDA Forest Service, Index of Species Information 2008.

Wetmore, A. 1956. Birds of the Pleistocene in North America.  Smithsonian Miscellaneous Collections 138(4): 1-24.

The Pleistocene mass-extinction left a number of plants and animals ill-adapted to modern life—trees with fruit or seeds too large to be swallowed and transported (Janzen and Martin, 1982), with outmoded defenses (Barlow, 2000), or waiting endlessly for agents of disturbance that are no more.  They are the survivors of vanished communities, still reflecting the forces under which they evolved for hundreds of thousands of years, and often in decline today.  They are the ghosts and orphans of the Ice Age.  I have seen an ice age ghost, and it’s a nightmare!  (image borrowed from)

The Osage Orange (Maclura pomifera) is often cited as one of North America’s more conspicuous ice age orphans for its outsized fruit (Barlow, ibid.).  About fifteen years ago I planted a small specimen and made the mistake of pruning off a couple of branches to encourage it to grow into a more open form.  I awoke a demon that had been sleeping inside for 12,000 years—its “rapid sloth-defense” genes.  The tree swiftly grew a thick barricade of stout upright, ferociously spiny branches, attempting to protect its crown—exactly what I was trying to avoid. The branches are up to 12 ft. long and straight as a fishing pole, 3/4 inches in diameter at their base, with inch-long needle-sharp thorns.  Now once a year I take my life in my hands and climb a ladder, pruning shears in hand, and try to negotiate some openness with this plant.  It’s a losing battle, and always bloody.  Its thorny stockade now stretches to the top, at least twenty feet high now–far beyond the reach of white-tailed deer.  This defense evolved with taller and tougher browsers in mind— North American camels, mastodons and sloths.  I can only imagine what the tree is thinking. . . Why won’t this stupid sloth take a hint and go away!!   My hope is that it will eventually grow tall enough and decide its apical buds are safely out of my reach and stop expending energy on this living razor-wire. Heaven help me though if it has mistaken me for an Eremotherium, North America’s biggest ground sloth.  Standing on two legs it could probably have reached at least 30 feet high.  I may be in for a long and painful battle.

Plants defend themselves from herbivores by many different means both chemical and physical.  The defenses may be constitutive, i.e. present whether herbivores are around or not, or induced, i.e. a direct response to herbivore damage.   Constitutive defenses can vary between different parts of the plant depending on the risk, and with the plant’s maturity.  Defenses are costly to a plant, diverting energy away from growth and reproduction (Gomez and Zamora, 2002).  That’s believed to be the force behind the evolution of induced defenses—save your energy until you need it.  A plant’s induced reactions are also affected by its physical condition, energy reserves, and the resources available from its environment (Bergelson and Purrington, 1996).  In theory plants should suffer a setback due to browsing but some respond with spurts of vigor, so-called overcompensation, and seem to benefit and even depend on browsing (McNaughton, 1983) (Paige and Whitman, 1987).

M. pomifera has evolved a complex multi-layered defense that is both chemical and mechanical; constitutive and induced.   As the tree grows naturally it arms its branches with a minor scattering of thorns, no more menacing than a rose’s. They force browsers to forage more slowly, to take smaller bites, and to spend more time manipulating leaves and shoots in their mouths in order to chew and swallow them comfortably.   As handling time increases, the net benefit to a browser of eating the plant decreases.  If the leaves are small, and especially if the foliage isn’t highly nutritious, and there are alternative food plants, many browsers limit their munching to levels the plant can live with (Cooper and Owen-Smith, 1986).

Only under severe browsing pressure (or pruning apparently) do some plants like M. pomifera call out the big guns.  The blitz of protective limbs is called adventitious branching, and the counterattack may be both physical and chemical. The prickles on Rubus species grow back longer and sharper after being browsed (Abrahamson, 1979). Browsed European holly (Ilex aquifolium) leaves grow back with extra prickles (Obeso, 1997).  Young (1987) found Acacias increased the length of their new thorns in response to browsers, but relaxed the response after their prolonged departure (Young and Okello, 1998).  Some plants use a combination of thorns and chemicals; for others, chemicals are enough.  Under severe browsing some Alaskan trees grow adventitious shoots with 2X the toxic resin concentration of their regular foliage, halting the browsing of snowshoe hares and leading to the recurring collapse of the hare population every ten years (Bryant, 1981).  

An anti-herbivore defense is a compromise for a plant.  There are many different kinds of browsers in the woods with many different sizes and shapes of mouths and tongues, and levels of experience.  No defense is perfect or effective against all browsers, especially insects.  Evolution leads a plant to anticipate its risks and plan its defenses appropriately—in the case of M. pomifera, a pattern of branching and arrangement of spines, combined with a biochemical arsenal, perfected through natural selection over hundreds of thousands of years.   So don’t tell me sloths are gone. . . we’re surrounded by  evidence of their presence. My Osage Orange tree knows there’s a sloth nearby (and a darn stubborn one too!) and it’s responding in every way it knows.  If I could only read its form and chemical reactions better–listen to it better–oh the stories it could tell me about sloths. . . . Dave

(photo by Phil Douglis)

References

Abrahamson, W.G. 1979. Patterns of resource allocation in wildflower populations of fields and woods.  American Journal of Botany 66: 71-79.

Barlow, C. 2000. The Ghosts of Evolution:  Nonsensical fruit, missing partners, and other ecological anachronisms.  Basic Books.  New York, NY.

Bergelson, J. and Purrington, C.B. 1996.  Surveying patterns in the cost of resistance in plants.  The American Naturalist 148: 536-558.

Bryant, J.P. 1981. Phytochemical deterrence of snowshoe hare browsing by adventitious shoots of four Alaskan trees. Science 213: 889-890

Cooper, S.M. and Owen-Smith, N. 1986. Effects of plant spinescence on large mammalian herbivores.  Oecologia 68: 446-455.

Gomez, J.M. and Zamora, R. 2002. Thorns as induced mechanical defense in a long-lived shrub (Hormathophylla spinosa, Cruciferae). Ecology 83: 885-890.

Janzen, D.H. and Martin, P.S. 1982. Neotropical anachronisms: the fruits the Gomphotheres ate.  Science 215:19-27.

McNaughton, S.J. 1983. Compensatory plant growth as a response to herbivory.  Oikos 40: 329-336.

Obeso, J.R. 1997. The induction of spinescence in European holly leaves by browsing ungulates.  Plant Ecology 129: 149-157.

Paige, K.N. and Whitman, T.G. 1987. Overcompensation in response to mammalian herbivory:  the advantage of being eaten. The American Naturalist 129: 407-416.

Young, T.P. 1987. Increased thorn length in Acacia drepanolobium—an induced response to browsing.  Oecologia 71: 436-438.

Young, T.P. and Okello, B.D. 1998.   Relaxation of an induced defense after exclusion of herbivores:  spines on Acacia drepanolobium.  Oecologia 115: 508-513.

We’ve received our preliminary reports on the fossil seeds and pollen from the site. The seeds are what you would expect to find in the backwater-areas of a river—wetland taxa and weedy types profiting from the local disturbances. The pollen report is intriguing though– oak, pine, cedar and hickory, with some more weeds and lowlanders tossed in.  A couple of things stand out—of course there are many different kinds of oaks and pines, etc., each with its own requirements, but generally they all need large doses of direct sunshine to grow.  Their seedlings don’t survive in the shade. We found the tip of one spruce needle, but this doesn’t add up to being a dense boreal spruce forest.  With oaks and hickories, etc., it feels a lot like the Iowa we know—different species possibly, but in form and type of trees, the landscape we inherited from the Native Americans 150 years ago.  (Photo borrowed from)

The Tarkio Valley was obviously a lot more diverse than this— most seeds and pollen don’t survive 12,000 years under ground, and plants differ markedly in the amounts they produce.  Seeds don’t travel as far as pollen so they provide a close-up picture of the site, albeit distorted by the varied dispersal mechanisms plants have evolved.  Water can carry seeds long distances, but the velocity of the water here was very low, so these seeds came from nearby.  Pollen provides a wide-angle view of the valley beyond its floor, but that brings other caveats.  A pollen count is more likely to pick up the trees that rely on the wanderings of the wind for fertilization–they have to be prolific.  Plants that use animal transporters (e.g. insects) can be more conservative, so they show up less often. Wind speed, direction and tree height all affect where and how far pollen travels.  Altogether, the reports paint a picture with some intriguing possibilities, and future opportunities. (Pollen  SEM’s borrowed from the National Pollen Aerobiology Research Unit.)

We can’t know for sure the exact texture of the Tarkio Valley uplands, but the pollen evidence points to the kind of open woodland that researchers say was widespread late in the Pleistocene (Wright, 1984).   Sunny open woodlands need something to keep them open though—moderate disturbances that kill swathes of mature trees on a regular basis.  There aren’t too many candidates—drought, floods, disease, high winds, lightning,/fires, and the residents themselves.  There’s a place for all of these in our Pleistocene disturbance regime, but Owen-Smith (1987) suggests the primary role was played by the megamammals in the community (i.e. weighing > 1 ton), as they do wherever they live in Africa today.   That would make Megalonyx one of the leading actors, along with mastodons and mammoths, in maintaining this woodland and making it possible for the oaks, etc., and many other species to thrive here.

Armed with the plant and tree lists, our knowledge about seed and pollen dispersal, and some reasonable assumptions about the missing pieces, including the Ice Age “orphans” and ”ghosts,” plus of course the omnipresence of these amazing sloths, we have the basis for developing an exciting and highly educational Ice Age park or garden.  Imagine  an interpretive trail with life-size models of the megafauna, with informative signs identifying the animals and various trees, and discussing their interrelationships.   The opportunity to address the topic of climate change at the end of the Pleistocene–humankind’s last experience with global warming–could serve as an unparalleled teaching tool for addressing our most serious contemporary environmental challenge. If such a park could be located near a river there would be the opportunity to add  a wetland  and riparian educational dimension.  It would be a compelling attraction and opportunity for commercial development . . . . But, there is a need in Iowa for more than this. We need real habitat protection, and ecological research into how best we can preserve and share our remaining natural lands with wildlife in the 21^st century. An ice-age-themed zoological park combining plants and animals could help accomplish that goal and provide a venue for researching some of our current ecological problems. (photo by Bret Rogers)

Oak trees are disappearing from Iowa today.   Oak seedlings need wide sunny openings to survive, but as our forests become overgrown with maples and other shade-tolerant species, life for the tenants on the ground floor is getting increasingly difficult. The reforestation of the eastern US is widely heralded, but the new growth bears little resemblance to the oak-pine-hickory woodlands there before European settlement.   There has been almost no reproduction of White Oaks for a century in the eastern half of the continent and little recruitment of most of the other major upland oaks for 50 years (Abrams, 2003). The potential impact on our native ecosystems is devastating. A vast number of plants, fungi, insects and other animals, and uncounted micro-organisms have evolved to live on, in and around oaks, and when their hosts vanish the survival of the entire community is jeopardized. The cause of the problem is rooted in the Ice Ages and the loss of animals like the sloth. (Photo by Bo Mackison)  To be continued.  Next time—disturbing thoughts. . . . Dave 

Cedar Rapids has released its plan for restoring the neighborhoods ravaged by this summer’s floods. I’m disappointed.  I was hoping for a bolder vision, something that recognized the increased likelihood of future floods and turned the riverfront in a more sustainable direction—like an Ice Age Zoological Park recreating the sloths’ habitat.  Besides serving as an important tool for education and research about Iowa’s truly natural environment (i.e. before Native American alterations to the land) and a valuable wildlife corridor, a natural environment park would bring significant commercial development opportunities, tourist revenue and jobs. A riverfront park could be designed to meet the Cedar River half way and work with its perennial floods instead of against them, like the truce Davenport, IA has forged with the Mississippi.  Restored wetlands, lakes and other containment basins could absorb water rather than speeding its way onward to create bigger problems for the communities downstream. Large urban zoological parks aren’t without precedent.  The 1,800-acre San Diego Zoo Wild Animal Park is one of the largest tourist attractions in southern California with attendance of 2 million visitors annually (Wikipedia, 2008).  Why not here? (image One Way Street by bpkelsey, borrowed from)

The preeminent role the extinct Pleistocene megafauna played in shaping the North American landscape has largely gone unrecognized here despite abundant corroborating evidence from across the ocean. The megamammals in Africa (i.e. animals > 1 ton, e.g. elephants, rhinos, hippos and large giraffes) play a keystone role in managing their habitats (Owen-Smith, 1988).  Elephants especially are constantly transforming the landscape.  By debarking and toppling large trees they create habitat for other animals, and open the forest floor to sunshine allowing a variety of other plants to flourish.  The flush of new growth paves the way for smaller animals to multiply.   Elephants and hippos create trails and dig wallows and water holes, providing the edges, corridors and microhabitats for fugitive species to settle in and the resources they need to survive. By transporting the fruit and seeds of select plants large mammals further encourage the diversity of the forest.  Mastodons, mammoths and ground sloths played a similar sweeping role in Ice Age North America (Soulé and Noss, 1998).

The loss of the Pleistocene mega-mammals has left us with a number of plants strangely ill-adapted to modern times, with seeds and fruits too large to be swallowed or transported and largely ignored by animals today (e.g. Osage Orange, right), or with profligate defenses that seem obvious over-kill with respect to contemporary threats (e.g. Honeylocust, left).  These characteristics only make sense when one considers the vanished herbivores with whom these plants evolved, and which disappeared just an evolutionary eye-blink ago. Barlow (2000) calls these dispossessed plants ice age ghosts and orphans.

Insects, birds and small mammals were affected as well –pronghorns, for example, have evolved to run 60 mph, but no North American predator can approach that speed.  A perplexing misallocation of biological resources by evolution until one considers the extinction of the North American cheetah, which presumably could run only 59 mph (Byers, 1997).  We are surrounded by these ice age reminders or “shadows,” and some very familiar species are facing serious challenges today now that the activities of the temporary stand-ins for the keystone megafauna, Native Americans, have been curtailed (e.g. burning). (image borrowed from)

The problem of disjointed ecosystems is particularly acute on the Great Plains where, bereft of native browsers and much to the consternation of its ranchers, the landscape is becoming overgrown with shrubs inedible to the favored species–cattle–non-natives, of course.  Scientists have proposed “rewilding” the region with surrogates for the missing megafauna from Africa and Asia (Donlan et al. (2006).  Proponents admit a tremendous amount of research needs to be completed before a horde of nonnative species is unleashed into the environment (Martin, 2005).

A rewilding experiment is progress now in Siberia.  Zimov is seeking to transform over 60 square miles of Arctic tundra to grasslands by establishing breeding populations of Alaskan musk oxen, Siberian ponies and Canadian woodland bison (Stone, 2001). He believes the grazing, trampling, and manure of the large animals will eventually result in the replacement of the tundra mosses by the short subarctic grasses, a community that vanished with the mammoths 12, 000 years ago (Guthrie, 1990).   Several less formal experiments are going on here in the United States with the protection of wild horses and burros on public lands in the West and the reintroduction of condors in the Grand Canyon, but no one has tried an experiment exploring the impact of mega-browsers on the Eastern woodlands.

Rewilding Iowa isn’t in the cards—the land is simply too valuable for farming.   Furthermore, the space available in the Cedar Rapids plan isn’t enough to accommodate large animals in sustainable numbers or the natural disturbance regime of the river, much less the landscape transformation power of megafauna like elephants, but a park could be expanded considerably beyond the downtown limits through a combination of  purchase, long-term leases and conservation of easements on connecting riverfront up and downstream.  In the face of an accute shortage of mastodons, Zimov plans to use bulldozers to mimic the ice age disturbance regime.  We might try black rhinos, giraffes and John Deeres. As Einstein once said, “If we knew what we were doing, it wouldn’t be called research, would it?” (Haynes, 2004).  A Cedar Rapids park would be uniquely positioned, sitting at the junction of three state universities with their considerable agricultural, biological and engineering research expertise. (photo by Phil Douglis, borrowed from)

Is an Ice Age Sloth Park possible?  Can we even begin to guess what Iowa’s forests looked like when the sloths were alive, or is an Ice Age Park just a fantasy like the late unlamented Coralville rainforest? Yes, it’s possible, and we don’t have to guess.  We have preliminary reports back on the seeds and pollen from the site.  They may provide a compelling picture of Iowa and the land the sloths called home.  More about the seeds and pollen next week. . . . Dave

References

Barlow, C. The Ghosts of Evolution:  Nonsensical fruit, missing partners, and other ecological anachronisms.  Basic Books.  New York, NY.

Byers, J. 1997. American Pronghorn: Social adaptations and the ghosts of predators past.  University of Chicago Press. Chicago, IL.

Donlan, C.J., Berger, J., Bock, C.E., Burney, D.A., Estes, J.A., Foreman, D., Martin, P.S.,, Roemer, G.W., Smith, F.A., Soule, M.E., and Greene, H.W. 2006. Pleistocene Rewilding: An optimistic agenda for twenty-first century conservation. The American Naturalist 168: 660-681.

Guthrie, RD. 1990. Frozen Fauna of the Mammoth Steppe:  The story of Blue Babe. The University of Chicago Press.  Chicago, IL.

Haynes, G. 2004. Rather odd detective stories:  a view of some actualistic and taphonomic trends in paleoindian studies.  Breathing Life into Fossils:  Taphonomic Studies in Honor of C.K. (Bob) Brain.  T. Pickering, K. Schick, and N. Toth (eds.)  Stone Age Institute Press. Gosport, IN.

Martin, P.S. 2005. Twilight of the Mammoths:  Ice Age extinctions and the rewilding of America.  University of California Press.  Berkley, CA.

Owen-Smith, R.N. 1988. Megaherbivores:  The influence of very large body size on ecology.  Cambridge University Press, Cambridge.

Soulé, M. and Noss, R. 1998. Rewilding and biodiversity: complementary goals for continental conservation. Wild Earth Fall, 1998: 18-28.

Stone, R. 2001. Mammoth:  resurrection of an ice age giant. Perseus Publishing.  Cambridge, MA.