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Coevolution of Cycads and Dinosaurs George E

Coevolution of Cycads and Dinosaurs George E

Coevolution of and George E. Mustoe* INTRODUCTION TOXICOLOGY OF EXTANT CYCADS cycads suggests that the biosynthesis of ycads were a major component of Illustrations in textbooks commonly these compounds was a trait that C forests during the Era, the depict herbivorous dinosaurs browsing evolved early in the history of the shade of their fronds falling upon the on fronds, but biochemical evi- Cycadales. Brenner et al. (2002) sug- scaly backs of multitudes of dinosaurs dence from extant cycads suggests that gested that macrozamin possibly serves a that roamed the land. Paleontologists these reconstructions are incorrect. regulatory function during cycad have long postulated that cycad foliage Foliage of modern cycads is highly toxic growth, but a strong case can be made provided an important food source for to vertebrates because of the presence that the most important reason for the reptilian , but the of two powerful neurotoxins and carcin- of cycad toxins was their of dinosaurs and the contemporaneous ogens, cycasin (methylazoxymethanol- usefulness as a defense against foliage precipitous decline in cycad popula- beta-D-glucoside) and macrozamin (beta- predation at a time when dinosaurs were tions at the close of the N-methylamine-L-alanine). Acute symp- the dominant herbivores. The protective have generally been assumed to have toms triggered by cycad foliage inges- role of these toxins is evidenced by the resulted from different causes. Ecologic tion include vomiting, diarrhea, and seed dispersal characteristics of effects triggered by a cosmic impact are abdominal cramps, followed later by loss modern cycads. a widely-accepted explanation for dino- of coordination and paralysis of the saur extinction; cycads are presumed to limbs. may result from acute liver CYCAD SEED have suffered because of their inability failure or starvation and dehydration DISPERSAL STRATEGIES to compete with fast-growing flowering stemming from paralysis (Whiting 1963, Seed dispersal is important to a that appeared during the mid- 1989 ’ survival for several reasons. Cretaceous “angiosperm explosion.” Adverse effects caused by cumula- Plants that are able to spread their This paper explores a different hypothe- tive low-dose exposures are less well seeds over a large area reap genetic sis, i.e., that the evolutionary fates of understood. Cycad ingestion by humans benefits from the opportunities for cycads and dinosaurs were inextricably has been proposed as a cause of amyo- cross-pollination among individuals that intertwined, and the Late Cretaceous trophic lateral sclerosis/parkinsonian come from differing gene pools. Seed extinction of these reptiles was the dementia complex (ALS/PDC), a fatal triggering event that caused cycads to neurogenerative disease prevalent in diminish to their present status as “liv- parts of Guam, , and Japan ing .” The main tenet of this hy- (Spencer et al. 1991; Spencer and Kisby pothesis is cycads depended on herbiv- 1992; Sacks 1997; Cox and Sacks 2002; orous dinosaurs to disperse their seeds, Brenner et al., 2003). Cycad toxins are and the disappearance of these herbi- mutagenic and they induce a variety of vores led to a precipitous decline in the cancers, particularly of the liver and geographic range and numerical abun- kidneys. Laboratory studies have impli- dance of cycads. Evidence comes from cated these compounds as a possible the toxicology of extant cycads, their cause of diabetes. The only creatures seed dispersal strategies, anatomical known to consume cycad foliage with characteristics of herbivorous dino- no discernible ill effects are a few types saurs, and the geographic distribution of insects, including Lepidoptera larvae and taxonomic diversity of modern and that utilize cycasin absorbed during cycads. feeding as a defense against predators (Nash 1992). The presence of cycasin and Fig. 1. Cross-section of seed cone of *Geology Department, Western Washington roezlii. Adapted from André (1873) *University, Bellingham, Washington 98225. macrozamin in all genera of modern L’Illustration Horticole 20, Planches 133-134, *([email protected]) reproduced in Jones (1993), p.301.

Fig. 2. Cycads evolved three basic architectural strategies for making their seeds available to large browsing : individual seeds attached to long, flexible (example: media), upright cones borne at the stem apex (example: manikensis), and cones suspended beneath the crown on a short stalk (example: spinulosum) (Photos by Bart Schutzman).

The Cycad Newsletter 30(1) March 2007 Page 6 dispersal also provides a mechanism for CYCAD/ COEVOLUTION dominant herbivores, and the geographic migration of popula- It is not a coincidence that the first group of dinosaurs to achieve great tions in response to changing environ- cycads acquired a combination of toxic numerical abundance and widespread mental conditions. Finally, most herbivo- foliage and large poisonous seeds that geographic distribution as evidenced by rous insects and microbial plant patho- are enclosed within edible fleshy tissue. fossils from Europe, Asia, Africa, and gens are able to infest only a few close- The simultaneous emergence of large North and (Galton 1985, ly related host species, and survival populations of cycads and herbivorous VanHeerden 1997). The absence of wear rates are much higher for seedlings that dinosaurs during the Triassic suggests facets suggest that prosauropods used sprout far away from the parent plants that these characteristcs resulted from their teeth for nipping off bits of vege- because distance inhibits the spread of a process of coevolution, where chemi- tation. They relied on to pests to the new generation (Janzen cal deterrents to foliage predation were abrade unchewed ingested matter, a 1970). combined with a sophisticated repro- style of that made prosauro- Cycads are prolific seed producers, ductive strategy that rewarded certain pods ideally suited for the dispersal of with individual cones containing 500 or reptiles for dispersing cycad seeds. High fertile cycad seeds. more large seeds (Fig. 1). Each seed concentrations of toxins in cycad ker- Sauropods became dominant herbi- consists of a hard starchy kernel sur- nels restrict seed ingestion to animals vores during the Era. These rounded by a thick fleshy sarcotesta. that are large enough to swallow them reptiles had larger bodies than prosau- The presence of a fleshy sarcotesta whole; seeds are unpalatable to small ropods, but both dinosaurs possessed contrasts to the naked seeds produced gnawing animals and to larger herbivores similar dental and digestive characteris- by other gymnosperms, and the mor- that masticate their food. Undigested tics. Stegosaurs, the other common phology of cycad seeds is functionally seeds excreted in dung benefit both Jurassic , likewise had teeth analogous to the fruit-borne seeds of from their dispersal to new and that were ill-suited for masticating foli- angiosperms. Stevenson (1990) and Bren- the excrement provides a supply of age. Rather than being selective feed- ner et al. (2003) provide a detailed dis- nutrients for juvenile plants. Dinosaurs ers, all of these herbivores consumed cussion of cycad and repro- benefited from this reproductive ar- huge quantities of plant matter, relying duction. The kernels of all extant rangement in two ways: cycad seed on microbial fermentation to digest to cycads contain high levels of toxins, but cones provided a nutritious treat, and digest cellulose (Weaver 1983; Farlow in almost all species the sarcotesta is the subsequent seed dispersal insured 1987). edible and posses characteristics that that future generations of cycads would Cycad seed cones were probably attract animals. The sarcotesta is so continue to supply this food source. never a major food source for herbiver- rich in sugar that members of many Modern cycads have stiff, often ous dinosaurs, the sugar-rich sarcotesta indigenous cultures savor this tissue for spinose fronds that deter browsing, but having provided a tasty snack rather its sweet flavor (Whiting 1963). Cycad seed cones are presented in a manner than the main course. Although some sarcotesta are typically bright colored, that allows herbivores to avoid the foli- kernels may have been crushed during often red, orange, or yellow, and they age. Cycad genera commonly bear up- digestion by the abrasive action of gas- are densely clustered in large highly right cones positioned above the leaf troliths, the massive body sizes of these visible cones that are positioned within crown (e.g., Dioon, Encephalartos, Lepi- herbivorous dinosaurs kept toxin levels easy reach of browsers. These bright dozamia, , , and below the amount necessary to cause colors likely evolved to attract reptiles, Zamia). In many species of Cycas the illness. which posses good color vision; except seeds are borne on flexible sporophylls The evolutionary fate of cycads took for primates, most are color that extend outside the protective a down-turn in the Late Cretaceous, blind. Although see colors, their fronds, and the large seed cones of when hadrosaurs and other ornithopods small body sizes make them ineffective and Dioon rzedowskii emerged as the dominant herbivores. dispersers of cycad seeds. dangle from a peduncle (Fig. 2). Al- These dinosaurs posessed banks of com- Although sarcotesta tissue is readily though cycad seeds are positioned so pound shearing teeth that allowed them digested, the kernel is protected by a that they can be easily reached by large to chew tough food with great efficien- resistant outer coating (sclerotesta) browsing animals (Fig. 3), toxins within cy. Cycad seeds would have been inedi- that insures safe passage of the en- the kernels can be avoided only if the ble for these dinosaurs because potent dosperm through the host’s digestive seeds are swallowed intact. This combi- toxins would have been released during tract. Horticulturists have learned that nation of properties probably evolved to mastication. Increased efficiency in cycad germination rates are greatly attract consumption by prosauropods, consumption of non-cycadaceous foli- improved when the sclerotesta is abrad- sauropods and stegosaurs (Fig. 4), her- age provided a ed with a knife or file (Smith 1978) and bivores that used their teeth to rake in nutritional when the seeds are soaked in concen- foli- age, which was swallowed after benefit that trated acid (Dehgan and Johnson 1983), little mastication mimicking passage of the seed through (Weishampel the digestive tract. Removal of the 1984). Prosauro- fleshy sarcotesta is an important prelimi- pods were the nary step because this tissue contains chemicals that inhibit germination (Jones 2002).

A BC Fig. 3. The heights and positions of cycad seeds appear to have evolved to make them easily accessible to herbivourous dinosaurs. A) stegosaur shown with Encephalartos lebomboensis; B) prosauropod shown with Cycas armstrongii; C) sauropod shown with Dioon spinulosum. Dinosaur sketches adapted from reconstructions by Farlow and Brett-Surman (1997). The Cycad Newsletter 30(1) March 2007 Page 7 offset the inability of these dinosaurs to that species such as Nilsonnia, , trends. Most species of Zamia are un- consume cycad seed cones. In addi- and had wide geographic derstory plants distributed sporadically tion, the rise of angiosperms offered a distribution. In contrast, the only Ceno- from Florida to Bolivia, but Z. pseudopar- rich new food source during the Late zoic having transcontinental dis- asitica is a rain forest epiphyte found Cretaceous. As a result of changing tribution is Zamia, found as fossils in only in one small area of Columbia. An- dinosaur dentition, cycad populations scattered formations from Wyoming to other highly specialized cycad, Z. roe- markedly declined, but the plants did Chile. Cycads grew in much of Europe as zlii, grows in brackish intertidal mud at not become extinct because a few late as the Miocene Epoch, but none a single area on the nearby coast (Saba- species of dinosaurs continued to dis- are native to the region today. In North to 1990). perse cycad seeds, albeit less effective- America, early Tertiary cycad popula- These occurrences reveal that ex- ly than the sauropod herds of earlier tions extended as far north as Alaska, tant cycads continue to respond to the times. The sauropod Alamosaurus sur- and from the California coast east to pressures of natural selection, but they vived in North America until the close of Missouri and Tennessee. Fifty million have achieved only very limited progress the Mesozoic, and diverse assortment of years later, only five cycad genera re- toward overcoming the problem of seed Upper Cretaceous dinosaurs included main native to the New World, restrict- dispersal. In the mountains of Mexico ankylosaurs and a few other herbivores ed to local regions of Florida and Geor- some Dioon populations take advantage that lacked efficient chewing ability. gia, the Caribbean Islands, Mexico, Cen- of gravity when their smooth ovoid The world-wide demise of dinosaurs tral America, and northern South Ameri- seeds roll downhill to colonize new at the end of the Cretaceous Era must ca (Jones 2002, Whitelock 2002). sites. Seeds of three species of Cycas have dealt a severe blow to cycads, who Though never a dominant constitu- have a layer of spongy tissue that pro- suddenly found themselves lacking any ent of Cenozoic forests, cycads are well vides buoyancy that permits them to be effective mechanism for seed dispersal. represented in Early Tertiary palefloras transported great distances by ocean As a modern analog, May (1977) and in North America. Hopkins et al. (1998) currents (Dehgan and Yuen 1983). Seed Temple (1977) attributed extinction of reported the presence of cycad leaf flotation has allowed C. circinalis and C. the dodo (Raphus cuculatus) as a cause fossils from twelve localities in Pale- rumphii to spread from the coasts of of the near-extinction of Calvaria major, ocene formations of Colorado and Wyo- India and Southeast Asia to , once an abundant tree in the forests of ming. Other cycads have been discov- Comoros, and Seychelles Islands. In . Calvaria seeds are enclosed ered in rocks of the Pacific contrast, Macrozamia communis forms within a thick endocarp durable enough Northwest (Manchester 1981, Hopkins dense coastal thickets in eastern Aus- to withstand being crushed during their and Johnson 1997). These early Tertiary tralia and Stangeria eriopus populations passage through the dodo’s powerful cycad fossils have two important char- are distributed along the coast of South gizzard, and these seeds germinate only acteristics: (1) foliar and cuticular char- Africa, but lack of seed buoyancy pre- after this coating has been partially acteristics indicate that they cannot be vents these cycads from reaching other abraded. Following the death of the last assigned to extant genera, and (2) each regions (Jones 2002). remaining dodo by hunters in 1681, leaf form typically occurs only within a Most modern cycads rely on birds Calveria populations declined precipi- single geologic formation, often restrict- and animals to disperse their seeds, tously. Quammen (1996) discussed a ed to a single locality. These features even though this process is usually not variety of factors that may have contrib- represent island-like biogeographic very effective. Crows, emus, hornbills, uted to this decline, but the disappear- patterns (MacArthur and Wilson 1967; ance of the island’s only large herbivore Quammen 1996) where isolated popula- likely played a major role. Other analo- tions gave rise to great taxonomic diver- gies can be found in Janzen and Martin sity, with each taxon having very re- (1982), who described the decline cer- stricted range. Lacking large animals to tain Central American plant species that disperse their seeds, cycad populations had evolved fruits to attract gompoth- became genetically isolated much like eres, ground sloth, glyptodonts, and populations of plants and animals that other large herbivores that became become separated by vast stretches of extinct during the Pleistocene. Subse- ocean. quent investigators reported similar Similar evidence can be found in the “neotropical anachronisms” from other distribution of extant cycad species, continents (Barlow 2000). which typically inhabit small areas where they occupy specialized ecologi- CYCAD SURVIVAL IN A cal niches. As an example, the Mexican DINOSAUR-FREE WORLD genus Dioon is comprised of eleven Warm, humid early Tertiary forests species and subspecies, each limited to provided suitable growing conditions for a small geographic range, with habitats cycads, but most of these populations that range from near sea level to above fell victim to global climatic cooling that 2500 m (Fig. 5). The environmental tol- began in the late Eocene. Episodes of erances of these individual populations unfavorable climatic change caused are quite varied. D. spinulosum and D. cycad populations to shrink, and in the rzedowskii both grow in moist habitats absence of large herbivores to disperse that have minimal temperature variation, seeds, these species were not able while other species of Dioon are re- migrate or to re-colonize their original stricted to arid regions that are subject their range when favorable conditions to large temperature fluctuations returned. Evidence of this process (Jones 2002) These plants all appear to comes both from fossil occurrences and have diversified from a common late Cenozoic ancestor (Sabato and DeLuca Fig. 4. of herbivorous dinosaurs that pos- from extant cycad populations. The sessed teeth suited for stripping vegetation that fossil record of Mesozoic cycads shows 1985). Other extant cycads show similar was swallowed with minimal mastication. The Cycad Newsletter 30(1) March 2007 Page 8 and are large enough to ACKNOWLEDGMENTS Galton, P. M. 1985. Diet of prosauropod swallow whole cycad seeds but other My interest in Cenozoic cycads was dinosaurs from the and early birds typically carry a single seed to a Jurassic. Lethaia 18: 105-123. kindled by leaf imprints discovered in Hopkins, D. J. Jr. & K. R. Johnson. 1997. nearby perch where they use their western Washington by W. L. Gannaway, First record of cycad from the to strip away the edible sarcotes- a dedicated amateur paleontologist who Eocene Republic Flora. Washington Geol. ta. Eckenwalder (1980) observed North- has contributed many specimens to 5(4): 37. ern Mockingbirds (Mimus polyglottos) Western Washington University. Com- _____, _____ and C. A. Jaramillo. 1998. enthusiastically feeding on seeds of ments on an early draft were graciously Diversity and evolution of Cenozoic cycads in western North America (ab- Zamia and Encephalartos at a Florida provided by J. O. Farlow, R. Geer, S. P. botanical garden, but the kernels were stract). B.S.A. Ann. Meeting, Baltimore, Girouard, Jr., S. R. Manchester, B. H. MD., Aug. 2-6, 1998: 75. dropped a short distance away. In natu- Tiffney, and W. C. Wehr. Janzen, D. H. 1970. Herbivores and the ral habitats, only 3% of Z. pumila seed- number of tree species in tropical for- lings were located more than 4 m from LITERATURE CITED ests. Amer. Nat. 104: 501-529. the nearest mature female plant. In Barlow. C. 2000. Ghosts of Evolution. Basic _____ and P. S. Martin. 1982. Neotropical many regions of the world, and Books, New York. anachronisms: the fruits the gom- small birds peel away the sarcotesta of Brenner, E.D., D.W. Stevenson & R.W. Twigg. photheres ate. Sci. 215: 19-27. nd 2003. Cycads: evolutionary innovations Jones, D. L. 2002., Cycads of the World, 2 cycad seeds, abandoning the kernels at ed. Smithsonian Inst. Press, Washington, the base of the host plant. Baboons and and the role of plant-derived neurotox- ins: Trends Pl. Sci. 8: 446-452. D.C. monkeys carry away intact cones, eat- Cox, P.A., & O.W. Sacks. 2002. Cycad neuro- MacArthur, R.H., and E. O. Wilson. 1967. The ing the fleshy pulp and spitting out the toxins, consumption of flying foxes, and Theory of Island Biogeoraphy. Princeton poisonous kernels. In Afrikaans, the ALS-PDC diseasde in Guam. Neurol. 40: Univ. Press, Princeton, NJ. common name for Stangeria eriopus is 767-772. Manchester, S. R. 1981. Fossil plants of the Eocene Clarno nut beds. Oregon Geol. bobbejaankes (“baboon food”), because Dehgan, B., & C. R. Johnson. 1983. Improved seed germination of Zamia floridana 43(6): 75-81. of the primate’s fondness for the cones May, R. M. 1977. Coevolution of Calvaria and (Whitelock 2002). African elephants have (Sensu lato) with and GA3 on germina- tion. Scientia Horticulturae 19: 357-361. the dodo. Nature 270: 204-205. been observed eating whole cones of _____ & C.K.K.H. Yuen 1983. Seed morpholo- Nash, R. J. 1992. The protective role of Encephalartos poggei, excreting the gy in relation to dispersal, evolution, and cycasin in cycad-feeding Lepidoptera. seeds a day or two later (Jones 2002). In propagation of Cycas L. Bot. Gaz. 144: Phytochem. 31: 1955-57. Mexico, seeds of Dioon are swallowed 412-418. Quammen, D. 1996. The Song of the Dodo: Eckenwalder, J. E. 1980. Dispersal of the Island Biogeography in an Age of Extinc- by deer, bears, and peccaries. However, tion. Scribner, New York. no modern can match the abili- West Indian cycad Zamia pumila L. Biotropica 12: 79-80. Sabato, S. 1990. West Indian and South ty of a browsing dinosaur that could Farlow, J. O. 1987. Speculation about the American cycads. Mem. N.Y. Bot. Gard. consume thousands of cycad seeds in a diet and digestive physiology of herbivo- 56: 173-185. single afternoon, and seed size and rous dinosaurs. Paleobiol. 13: 60-72. _____ and P. DeLuca. 1985. Evolutionary toxicity are phylogenetic constraints _____ and M. K. Brett-Surman, 1997. The trends in Dioon (). Amer. J. Bot. 56: 173-185. that restrict cycads to their present Complete Dinosaur. Indiana University Press, Bloomington. Sacks, O. 1997. The Island of the Colorblind status as botanical relicts. and Cycad Island. Alfred Knopf, New York. Smith, G. S. 1978. Seed scarification to speed germination of ornamental cycads. HortSci. 13: 438-439. Spencer, P. S., & G. E. Kisby. 1992. Slow toxins and western Pacific amyotrophic lateral sclerosis. Pp. 578-585 In: R. A. Smith, ed., Handbook of Amyotrophic Lateral Sclerosis. Marcel Dekker, New York. Stevenson, D., 1990. Morphology and sys- tematics of the Cycadales. Mem. N.Y. Bot. Gard. 57: 8-55. Temple, S.T. 1977. Plant- mutualism: coevolution with dodo leads to near extinction of plant. Sci. 197: 885-886. VanHeerden, J. 1997. Prosauropods. Pp 243- 263 In: J. O. Farlow and M. K. Brett- Surman, eds. The Complete Dinosaur. Indiana Univ. Press, Bloomington. Weaver, J. C. 1983. The improbable endot- herm: the energetics of the sauropod dinosaur Brachiosaurus. Paleobiol. 9: 173-182. Weishampel, D. B. 1984. Interactions be- tween Mesozoic plants and vertebrates: fructifications and seed predation. Neues Jahrb. Geol. Paleont. Abhandl. 167: 224-250. Whitelock, L.M. 2002. The Cycads. Timber Press, Portland, OR. Whiting, M. G. 1963. Toxicity of cycads. Econ. Bot. 17: 271-302. _____ 1989. Neurotoxicity of cycads, an annotated bibliography for the years Fig. 5. Geographic ranges of extant species of Dioon. Map based on data from 1829-1989. Lyonia 2(5): p. 201-270. Jones (1993) and Whitelock (2002). The Cycad Newsletter 30(1) March 2007 Page 9

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