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The Ghosts of Evolution

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As is often the case in my morning carpool to Kansas City, passions ran high when I raised the topic of megafaunal dispersal. George was at the wheel, I was riding shotgun, and Bob and Stan were scrunched up in the back of George's old Honda Accord. I was, to the best of my ability, explaining the arguments in Connie Barlow's new book about extinct seed dispersal partners: The Ghosts of Evolution. Connie asserts (along with veteran paleobiolists Paul Martin and Dan Janzen), that certain largish animals had big enough gullets to swallow fruits like Osage oranges whole and then poop out the seeds several miles away, thus expanding the plant's territory in the next generation. Unfortunately, nobody provides this service for Osage oranges anymore, which is why they all lie around rotting within a few yards of the mother tree every autumn.

In an attempt to confirm that a creature like a mastodon would willingly eat Osage oranges, Martin and Barlow persuaded the director of the Brookfield Zoo in Chicago to offer the fruit (scientific name maclura pomifera) to three of the zoo's elephants. "Affie, the matriarch of the Brookfield elephants, did eat maclura--but just the first fruit she was offered. After that, she showed no interest in any more. The reactions of the other elephants were strongly negative. One wasn't even willing to smell the fruit when the offer was first made. Finally, she took it from her keeper and hurled it down the hall. The second elephant did the same thing but aimed for the public area." I can't say that I blame them. As a child, I was under the impression that Osage oranges (or hedge apples) were poisonous.

Zoo elephants' finickiness notwithstanding, the book argues that some species are obviously "overbuilt" for the ecological niche they inhabit today. Why would natural selection lead to such an outcome? For example, pronghorns can run not just a little faster but way the hell faster than any of their nearest predators (wolves and coyotes). This speed is apparently a relic of days when something faster than wolves or coyotes were chasing pronghorns, possibly a New World cheetah that became extinct thirteen thousand years ago. Well, you may ask, why haven't the pronghorns slowed down and devoted their evolutionary energy to something more productive, like jumping barbwire fences? More generally, what is a believable schedule on which a species reacts to changes in its environment?

As Connie Barlow analyzes the results of experiments with the exotic fruits and seeds in her New York apartment kitchen, she writes with delight and authority. She teaches us technical and colorful terms such as seed predator and pulp thief. The former destroys seeds by eating them rather than by defecating them intact. The latter eats the flesh around the seed and discards the seed without transporting it to a promising new sprouting site. We humans are guilty of both depredations, although with our compost heaps we have introduced a modest new dispersal path for domesticated fruits. Barlow's story is certainly not bereft of poetic lyric, as in the "paucity of pawpaw pollinators"--or of Conan Doyle-ian suspense: "Perhaps the most compelling evidence that Mrs. Foxie defecated persimmon seeds intact can be found in my collection of fox feces."

In her final chapter, Barlow preaches the gospel of "the great work:" the purposeful and painstaking reversal of the appalling history of extinction for which our species has, knowingly and unknowingly, been responsible. If the dedication to and passion for nature that is evident in this book can infect an emerging generation of professional and amateur naturalists, we may within our lifetimes see the beginning of this work.

This splendid addition to the popular scientific literature is almost as insightful and as well written as David Quammen's "Song of the Dodo". A fine overview of Dr. Paul Martin's and Dr. Daniel Janzen's pioneering work on "ecological anachronisms" in New World plants, it should be read by ecologists and evolutionary biologists, as well as the scientfically interested public. Connie Barlow has made an important contribution to Martin's and Janzen's ideas by distinguishing relative degrees of ecological anachronisms. Yet her book does contain some serious omissions and factual errors which I shall note later. Let me first sing its praises.

Connie Barlow's overview of "ecological anachronisms" is absolutely superb. She has a tremendous eye for detail, but never gets completely bogged down by it. Instead, much of what she writes is replete with insightful humor. She opens with an excellent history of Martin's and Janzen's work. Her vivid writing is a wonderful synthesis of science, natural history and biography all thrown in for good measure. I suspect historians of science interested in ecology and evolutionary biology will turn to this book as a primary reference on "ecological anachronisms".

Readers will find compelling Connie Barlow's descriptions of Paul Martin and Daniel Janzen. She treats them as a dynamic pair passionate about their unique insights into ecology and other aspects of evolutionary biology. They will also find compelling her attempts at scientific research. I suspect they will chuckle as much I did while reading about her experiments on "ecological anachronisms" in the wilds of New Mexico and the urban jungle that is New York City.

Having sung some praises, let me point out some flaws. Robert MacArthur, the greatest ecologist of the late 20th Century, is tossing in his grave, hearing from Connie Barlow that evolutionary ecology is a new science. At the time of his death in 1972, he recognized the importance of history - or rather, "deep time" - in understanding ecological patterns. Indeed, he covers evolutionary ecology in the final chapter of his text "Geographical Ecology", an elegant synthesis and literary epitaph to his career. One of MacArthur's former graduate students, Dr. Michael Rosenzweig, a colleague of Paul Martin's at the University of Arizona, has looked upon paleontology as the source of interesting questions relevant to ecology which many ecologists don't have training, interest, or time to pursue. His interest has spanned decades, culminating in his "incumbent replacement" hypothesis on the role of adaptation in promoting "evolutionary success" in clades (groups of related species that share a common ancestor) that was published in 1991 in the scientific journal Paleobiology.

"Devolution" is a scientifically inaccurate term which Connie Barlow mentions several times, most notably on pages 220-221. What she describes as devolution sounds a lot like neoteny to me. In neoteny, juvenile features are retained by adults through natural selection. It's possible that natural selection will act to promote the production of smaller fruit in succeeding generations, as the result of neoteny, not "devolution." Stephen Jay Gould's "Ontogeny and Phylogeny" provides an excellent description of neoteny and other evolutionary trends related to changes in size and shape. Indeed, I wish she had shown him her manuscript prior to its publication. His insightful comments on "devolution" and adaptation - or rather aptations - would have made this a better, more scientifically accurate, book. Indeed, one minor failing of this book is that she glosses over the significance of adaptations/aptations/exaptations as a key towards understanding ecological anachronisms which a scientifically literate public might miss easily.

Despite my strong reservations, I still enthusiastically endorse this book. Its excellent coverage of "ecological anachronisms" should be long remembered.

E. O. Wilson writes, "Our species and its way of thinking are a product of evolution, not the purpose of evolution." Connie Barlow's "The Ghosts of Evolution" is an eloquent gift to all of us who yearn to discover more about the great adventure that is the evolutionary saga. The mystery at the center her book connects the reader in a profound way to the unfurling of evolution, to extinction, and to those who "remember" in their limbs and organs ancient relationships with beings long departed. Be ready for a whirlwind ride that will transform the most familiar and mundane details of our present world and plunge you into a Pleistocene universe where rhinos and camels roam ancient American deserts, giant 20-foot ground sloths lumber with gaping mouths toward tropical fruits, and mammoths and mastodonts rumble among themselves while browsing in the avocado trees and crunching honey locust pods against their enormous teeth. With some help from the author, we are quickly seeing evidence of this continent as it was before history, before humans, when the trees evolved to disperse their young through the bowels of their partners, the giant mammals, reptiles, dinosaurs, and birds. This was a world of creatures with gapes large enough to take in an entire fruit, swallow the pit intact, and plant it amid a steamy pile of fertilizer. While we no longer live among those giants, we are sojourners among their partners, the "anachronistic" plants, trees, and fruits that recall a world that, from our human perspective, ceased to exist between ten and twenty thousand years ago. As Barlow tells the story, "An avocado sitting in a bin at the grocery store is thus biology in a time warp. It is suited for a world that no longer exists. The fruit of the avocado is an ecological anachronism. Its missing partners are the ghosts of evolution." The "ghosts" from our past haunt the pages of Barlow's book and eventually drift into our modern world. Her book has crept into my head and now follows me down the grocery aisles, resurrecting enormous megafaunal ghosts who stalk the avocadoes and papaya bins. Who was Honey Locust seducing when she wrapped her seeds in foot and a half long pods dangling from the tops of her lacy limbs? No one who is here today, that's for sure! And so Honey Locust waits for a ghost, probably the elephant doomed by our ancestors at the end of the last Ice Age.

"The Ghosts of Evolution" is a science book that explores the new field of evolutionary study surrounding surviving anachronisms and extinct creatures. For a nonscientist such as myself, there is an enormous amount of information about the ways in which plants and animals interact to produce new generations. The book is also full of stories about the scientists themselves and the studies that have produced this knowledge. The stories are told with undaunted enthusiasm, a persistently inquisitive spirit, and a wonderfully eccentric sense of humor. As e-mails and counter-arguments shoot back and forth among the experts, Barlow sifts and winnows the results and produces them for us in a masterful style full of wit and humor and "in your face" common sense. I laughed through much of the book. Some of my favorite moments are when the author conducts her own experiments, using any and all available means to test her own theories and questions, her kitchen sink, her neighbor's horses (Pleistocene returnees to their home continent!), her resident fox and mice, her own alimentary system (careful always to chew and spit out the plants who use poisons to protect themselves!) In a museum in New York City, with the help of the director himself, Barlow reunites osage orange with the molar of its missing partner, the ancient Mammoth. The author's documentation is solid and thorough; her skill in incorporating and analyzing the literature that bolsters her book results in a delightful reading experience without a single stuffy or dull moment.

Amid the theory, the science, and the fun, a poignant message emerges about extinctions and the role we humans have played and will continue to play in the epic of evolution. Throughout her book, the author speaks in the voice of a scientist/writer on behalf of the "trees who remember" their extinct partners. At the end, however, Barlow crosses that scientific boundary to enter the realm of ritual in a moving memorial service to the missing Mammoth. The creator of the ceremony, fellow scientist Paul Martin, writes, "The service ended with a moving soliloquy from a Ms. Honey Locust of New York City. Ms. Locust sported a green hat bedecked with long, spiraling pods. Honey Locust trees may be streetwise, we learned, but their pods miss the megafauna." The final voice we hear springs straight from the hearts of Ms. Honey Locust and her advocate, Connie Barlow. On behalf of the ghosts, we are asked to remember the world as the trees remember, to find our human place among the widows and the bereaved, to enter a ritual time. Barlow delivers a final passionate plea to all of us to fulfill an evolutionary role we inherit as a result of the loss of the ancient mammals. "Thirteen thousand years ago, the responsibility for dispersing edible, large-fruited plants in the Americas fell to the humans. The present demands another profound passage in stewardship. . . When will we put an end to this saga of loss upon loss and resolve to undertake what [Thomas] Berry calls `the Great Work' of ecological and evolutionary restoration?" When, indeed?

"The tusks that clashed in mighty brawls
Of mastodons, are billiard balls..."
--from a poem by Arthur Guiterman

The exciting idea in this book is that there are trees that "lament" the passing of the mastodons and the other extinct megafauna that once distributed their seeds. What animal now regularly eats the avocado whole, swallows the seed and excretes it far from the tree in a steamy, nourishing pile of dung? No such animal exists in the Western Hemisphere to which the avocado is native. (Barlow reports that elephants in Africa, where the avocado has been introduced, eat the avocado and do indeed excrete its pit whole.)

How about the mango with its pulp that adheres so tightly to the rather large pit? As Barlow surmises, such fruits were "designed" for mutualists that would take the fruit whole and let the pit pass through their digestive systems to emerge intact for germination away from the mother tree. Note that the avocado pit is not only too large to pass comfortably through the digestive system of any current native animal of the Americas, but is also highly toxic so that such an animal would have quickly learned not to chew it. Note too that the mango pit is extremely hard, thus encouraging a large animal to swallow it along with the closely adhering pulp rather than try to chew it or spit it out. Consider also the papaya. The fruit are large and soft so that a large animal could easily take one into its mouth and just mash it lightly and swallow. Note too that the fruits of the papaya tree grow not high in the tree, nor is the tree a low lying bush. Instead the tree is taller than a bush but its fruits are clustered at a height supermarket convenient for a large animal to pluck.

Barlow considers a number of other trees, the honey locust and the osage orange, for example, as examples of ecological anachronisms, trees that have out-lived their mutualists and consequently must form new partnerships with other seed distributors or face extinction. For those trees that have pleased humans, the avocado, the mango, the papaya, etc., there is no immediate danger, but some other trees are at the edge of extinction. Their fruits fall to the ground and stay there until they rot. New trees grow only down hill when an occasional flood of water moves their fruit to a new location.

Barlow also sees ghosts from the Mesozoic era. She writes, "Ghosts of dinosaurs are easy to conjure in October and November wherever city landscapers planted ginkgo trees...even when I forget to look for the ghosts of dinosaurs my nose alerts me to their presence. Only a carrion eater could find the odor of fallen ginkgo fruit appealing. Before beginning this book, I wrongly blamed the alcoholic homeless for the vomitlike stench in Washington Square Park." (p. 12)

In short this book is about those trees--anachronisms--have been without their mutualists since the mass extinction of the megafauna of the Western Hemisphere that took place about 13,000 years ago. It is a popular expansion on some original work done by ethnologist Daniel H. Janzen and paleontologist Paul S. Martin, their seminal paper appearing in the journal Science in 1982. Connie Barlow's prose is not only very readable, but is full of the excitement of scientific discovery, vivid and concrete, and packed with an amazing amount of information so that not only the trees described, but the giant sloths, mastodons and mammoths--the ghosts of harvests past--come alive on the pages.

What Barlow does more than anything is open our eyes to the ecological nature of fruit and the relationships that exist between trees and the animals that eat the fruit. We learn how color, taste, aroma, texture, nutritional value, toughness of rind, size, shape, number of seeds and how they are encased, etc.--how all these qualities of fruit have evolved to entice the animals that will faithfully distribute the seeds, but also how some qualities discourage other animals, "pulp thieves" or "seed predators," that benefit from the food provided by the tree, but do not help in its propagation.

The story of the desert gourd was of particular interest to me because during many walks in the chaparral and deserts of California I have come across this vine with its hard, dry and unattractive gourds that were never picked or eaten. Barlow theorizes that the plant is also an anachronism, and that there did exist in the past animals that found the gourds, if not delicious, at least palatable.

Another curious anachronism reported on is the devil's claw of the Chihuahuan desert of Mexico. This plant produces a most amazing apparatus that wraps itself around an animal's foot and claw-like clings to the animal, dribbling its seeds to the ground as the animal moves. There is a photo of the claw on page 151 wrapped around a human ankle. Incidentally, the text is enhanced by a number of interesting black and white photos of the trees and their fruits.

This is one of the most interesting and original books on evolution that I have read in recent years, and one of the most informative.

I burned three pieces of French toast while browsing around in Ghosts of Evolution. If the statement "Connie Barlow eats hedge apples" appeared on the wall of the men's room at the Field Museum of Natural History, I would normally have dismissed it as a tasteless slur on a slow graffiti day. But because I have actually read the book, I knew the shocking truth. Connie actually has chewed on the pulp of the Osage orange and lived to tell about it. In fact, she gamely asserts that something way too big to fit into the men's room routinely chowed down on these fruits (and many others) back in the Pleistocene period: American mastodons. And just to bring the point home, on page 183 she shows us a picture of an Osage orange fruit resting on the molar of Mammut americanum. It looks like a mere gum ball on that humongous jaw.

So what, you say. Who cares? People who want to know the truth. People who stop talking on their cell phones long enough to look at a honey locust pod and not see something boring or annoying that needs to be cleaned up, but instead a naturally-posed puzzle that is more exasperrating than "White to move and mate in three moves" in a chess column. "I'm here," the pod is saying, "but why? My seeds are so tough that ants and birds don't give them a second look. The seeds won't even germinate unless they have been vigorously scratched up. And yet I manufacture a honey in the pod that would be a great meal for a hungry animal." What's missing in this picture? Connie Barlow, reporting on the research of Dan Janzen and Paul Martin, makes a strong case for ghosts, the megafauna that once roamed our landmass but which were wiped out by Guess Who back when there was still a land bridge between Asia and the Americas. I'm still devouring this book and already have friends trying to grab it away from me. I like the fact that it is in first person, and that Connie doesn't write stuffy prose. For example, "We might hope to find a seed in a coprolite, but whose turd is that anyway?" This is science journalism at its best, and it provides my first believable explanation of why hedge apples are so useless.

That's what Barlow writes about in this read-in-a-day work. A popular science account of evolutionary biology, mostly in Quaternary North America, it explores the co-evolution of plants and animals. She points to traits like large size, seed retention, digestion tolerance, and abrasion tolerance as indicative of megafaunal dispersion and thus identifies megafaunal fruits -- pawpaw, avocado, guava, papaya, passion fruit, cherimoya, desert gourd, honey locust, and Kentucky coffee. Next the author considers the various recently extinct North American species (horses, mastodons, tapirs, sloths, camels, giant tortoise) and which might have been interested in the various fruits. An interesting background discussion compares and contrasts foregut (ruminants like cattle, deer and sheep) and hindgut (like horses and elephants) feeders.

"Ghosts" reinforces the sense I've had since visiting Africa that North America is empty of some large and important creatures that should be here. I can now better visualize what plants they were eating, and what their preferred habitats were like. I can also better visualize the cascade of extinction, past and present, from animal extirpations to the plants that evolved with and depended upon them.

This book should change the way you look at the trees around you. At least it did for me.

Animals depend on plants, directly or indirectly. And sometimes the dependence can be very direct. Review the case of the spotted owl. But what is less understood is that sometimes a plant species can depend equally directly on one or more animal species. And if the animal species go extinct, the corresponding plant can be facing a big problem, particularly with regard to seed dispersal. No functional dispersal mechanism and the avocado not only falls close to the tree, but rots there as well. Not good design. How do these species persist? How do we recognize them? Barlow uses a variety of evidence - primarily species of trees that produce seeds over-engineered in any of several ways for the animals now available to disperse them - to make her case. She cites a number of North American and tropical species that are hanging on through tenuous alternatives: spreading by sucke!ring, by flooding, or by enlisting the assistance of the most mobile animal extant, the human mammal.

The style suffers from a bit of repetition, leaving the reader with the sense of a good long magazine article inflated to fill two covers.

But my sense is that anyone who is interested in the many and odd ways the pieces of the natural world fit together would find this book a rewarding read. I certainly did.

It is a story I never dreamed of; the story of how the fruit I love to eat got that way. THE GHOSTS OF EVOLUTION is a readable, engaging, and wonderfully informative story about the relationship of fruits, nuts and seeds to the animals that evolved with them. For example, the avocado. What kind of animal would have evolved with the avocado? Why did the avocado develop such a big seed? Why is is so juicy and inviting? Because animals long gone extinct in the Western Hemisphere evolved with the avocado tree, animals like the extinct elephants and others who disappeared around 15,000 years ago. Ms Barlow writes with a combination of racy, easy going wit and a respect for what scientists do. At the same time she is not above trying a few experiments of her own in her kitchen and on the streets of Manhattan. Superb.

Follow Connie Barlow's lead. Next time you're at the grocery, spend some time in the fruits and veggie section. Pick up an avocado, hefting it in your hand. You can feel the weight of that huge seed within. Compare it with the nearby oranges or apples. Mum warned you not to swallow the seeds when you were a child, remember? Trees would sprout in your tummy. No worries about trying to swallow that avocado seed, is there? While you're squeezing that avocado, think back on autumn skies sparkling with maple or sycamore seeds fluttering in the chill winds. Why the absurd difference in size? Is it important?

Connie Barlow thinks these differences are very important. As she reminds us, all those fruits have been around since long before humans confined them to orchards. Winged maple seeds can flit about on the mildest breeze. The avocado, however, clearly needs a little help finding a sprouting site. Before orchardists, who was there to help it reach one? Trees don't like to just drop seeds and hope for the best. Too many seeds in one place results in choking thicket or a sunlight-blocking canopy. The key is dispersal. Leave home, kids, and start life somewhere else. But a rock-sized hunk like an avocado or a honey locust needs a lift. Who gave ancient avocados a ride to a new home?

According to Paul Martin and David Janzen, the carriers were animals who don't exist any more. Barlow follows this pair of researchers who began a new scientific quest by wondering why jungle fruit was rotting under Costa Rican trees. All life struggles to continue through succeeding generations, and lying on the ground covered in fuzz doesn't bode success. Janzen thought there was something missing - an animal that might have conveyed the fruit elsewhere to launch the new generation. As they studied the problem, according to Barlow, they concluded that many fruits and their seeds are living on borrowed time. The animals that helped disseminate seeds for many trees are long extinct.

Barlow belongs at the head of the class for understanding and explaining how evolution works. She shows there's more to the story than tracing single lineages with subtle adjustments in limb, leaf, or mass. Plant life has coevolved with animal species. In developing defenses against animals eating their foliage, plants also needed allies to spread new sprouts. Some seeds travelled with thorns, but others were oversized for that means. Big seeds had to be swallowed, some to be passed intact with dung, but others to initiate the germination process within the gut before passage. All these mechanisms are specific, but the loss of partners have left many tree species vulnerable. Some have "second string" dispersers, but these may not be adequate.

Barlow guides us around the planet and through time, introducing us to trees, their fruits and their likely seed dispersing partners. She reminds us that North America evolved the horse, the camel and a variety of other animals that are either missing or were re-introduced. In those days, the American camel had two sets of incisor teeth. Current Old World camels have a lower set and a hard plate above. New Zealand had no large mammals. Who conveyed the seeds of fifty four species of divaricate plants around the islands? Probably the eleven extinct species of moa native to the islands. Why do some trees around the world have thorns that cease growing above a certain height? There used to be taller animals that could reach the fruits convey them away. Why did the digestive tracts of horses and cows evolve differently? They both eat grass. Barlow examines these and other questions with exquisite style, showing where the evidence shows well and where further work is required. And there is plenty for the young researcher to consider following.

If the findings of the past weren't surprising enough, Barlow's proposals for the future will leave many astounded. Especially farmers and ranchers. Elephants on the Prairies? Camels in Utah [they were there once, why not again?] Hand planted trees where the natural dispersers have disappeared? These are serious questions, because extinction isn't an isolated event. Barlow points out the "cascade effect" engendered by all extinctions. There are many important reasons to read this book. It may amaze you, but be reassured you will not be bored.

The premise of "Ghosts of Evolution" is that certain plants show traits that only appear logical if one presumes now-missing commensals - in this case, the vanished megafauna of North and South America. The original idea was proposed by Dan Janzen and Paul Martin in a famous paper co-authored in 1982. Ms. Barlow writes of her own efforts to find and understand these anachronisms, which are interesting and at times ingenious.

In spite of this excellent premise, the book suffers from three shortcomings, only one of which is major:
First, and most serious, the concept is appropriate for a shorter book. Many passages are repetitive and add little to the overall argument;
Second, there are too many personal anecdotes, even for a popular science work;
Third, exclusive use of the metric system detracts from the reading experience. English measure may no longer be acceptable in the scientific community, as Ms. Barlow states, but this book is directed to a non-scientific American audience. Putting the English measure in parentheses by the metric would improve readability.

In summary, an intriguing idea and a basically enjoyable read.