Coevolution of Cycads and Dinosaurs George E
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Coevolution of cycads and dinosaurs 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 Mesozoic Era, the depict herbivorous dinosaurs browsing evolved early in the history of the shade of their fronds falling upon the on cycad 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 herbivores, but the extinction of two powerful neurotoxins and carcin- evolution 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 Cretaceous 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. Death 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 plants that appeared during the mid- 1989 species 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, New Guinea, and Japan ing fossils. 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 fossil 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 Zamia roezlii. Adapted from André (1873) *University, Bellingham, Washington 98225. macrozamin in all genera of modern LIllustration 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 animals: individual seeds attached to long, flexible sporophylls (example: Cycas media), upright cones borne at the stem apex (example: Encephalartos manikensis), and cones suspended beneath the leaf crown on a short stalk (example: Dioon spinulosum) (Photos by Bart Schutzman). The Cycad Newsletter 30(1) March 2007 Page 6 dispersal also provides a mechanism for CYCAD/DINOSAUR COEVOLUTION dominant Triassic herbivores, and the geographic migration of plant 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 South America (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 gastroliths 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 digestion 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 Jurassic 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 herbivore, likewise had teeth analogous to the fruit-borne seeds of from their dispersal to new habitats 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 anatomy 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, Macrozamia, Stangeria, 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 mammals are color that extend outside the protective a down-turn in the Late Cretaceous, blind. Although birds see colors, their fronds, and the large seed cones of when hadrosaurs and other ornithopods small body sizes make them ineffective Dioon spinulosum and Dioon rzedowskii emerged as the dominant herbivores. dispersers of cycad seeds. dangle