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Ecology, Paleobiology and Evolutionary Constraint in the Octopus

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Ecology, Paleobiology and Evolutionary Constraint in the Octopus BULLETIN OF MARINE SCIENCE, 49(1-2): 245-255, 1991 ECOLOGY, PALEOBIOLOGY AND EVOLUTIONARY CONSTRAINT IN THE OCTOPUS Richard B. Aronson ABSTRACT Packard (1972) proposed that the evolution of the coleoid cephalopods was largely a response to competition and predation from vertebrates in the Mesozoic. While recent pa- leontological discoveries necessitate modifying this scenario, it remains true that the shell- less condition, streamlined body form, visual acuity, closed circulatory system, and denning, body patterning and other complex behaviors help octopuses avoid their teleostean predators and persist in shallow, nearshore environments. There is currently no experimental evidence that teleost-octopod competition is important in shallow marine communities. However, field studies suggest an inverse relationship between predatory fishes and octopus population density. Where predatory fishes are absent, in a semi-isolated marine lake in the Bahamas, octopuses are two orders of magnitude more abundant than in Caribbean coastal commu- nities. Octopuses are the top carnivores in the lake, where a constraint of morphological and behavioral evolution becomes important: dens are the limiting resource. Living in dens is also an evolutionary imperative in Caribbean coastal communities, but dens are plentiful and predation is limiting. Predation in the geologic past molded morphologies and behaviors well-suited to current, high-predation environments. These features become ecological con- straints when the usual limitation of heavy predation pressure is lifted. I suggest using a modified version of Packard's scenario to organize and guide future research on octopus ecology and ethology. In 1972 Andrew Packard proposed that the unique morphology, physiology, ecology and behavior of the coleoid cephalopods evolved in response to com- petition and predation pressure from vertebrates in the Mesozoic. Yet despite Packard's (I 972) interesting and provocative suggestions, and the fact that a great deal of research on Nautilus is directed toward answering paleobiological ques- tions, few coleoid ecologists or ethologists have attempted to view their results within the context of cephalopod evolution. Fewer still have considered how the evolution of coleoids fits into the "big picture" of global biotic upheaval-mass extinction and biological revolution-in the Phanerozoic. To honor the memory of Gilbert Voss, I think it most appropriate to synthesize what we know about how coleoids fit into ancient and modern benthic commu- nities, and how their current role in nearshore environments is intimately bound to their evolutionary history and that of the rest of the marine biosphere. Most nearshore, community-level field studies have involved Octopus spp., and so octopuses will be the focus of the ecological portion of this discussion. This paper will attempt to contribute an evolutionary framework within which to view pre- vious studies. It should also help direct future efforts toward achieving a broad understanding of the class Cephalopoda. I begin by reviewing Packard's (I 972) scenario, which still has great explanatory value despite the necessity of some major revisions. I discuss his scenario as a manifestation of the general trend toward predator-prey escalation in the Meso- zoic. I then consider the advantages and constraints of the coleoid life mode, as exemplified by the octopus, in dealing with the ecological pressures of shallow benthic communities. Finally, I put forth some suggestions for further research. 245 246 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991 PACKARD'S SCENARIO AND THE MESOZOIC MARINE REVOLUTION Packard (1972) gave a detailed account of the remarkable convergence between coleoid cephalopods and teleostean fishes. The streamlined body, closed circu- latory system, large brain, and chromatophore system are among many features shared by these two groups. The recent discovery of a lateral line analogue in squids (Budelmann and Bleckmann, 1988) is yet another example of how "fish- like" the coleoids are. Like many teleosts, coleoids are fast-moving, visual pred- ators. They use complex behavioral repertoires in prey capture, predator avoid- ance, and reproduction (Yarnall, 1969; Wells and Wells, 1972; Messenger, 1977; Packard and Hochberg, 1977; Wells, 1978; Moynihan and Rodaniche, 1982; Moynihan, 1985; Hanlon, 1988; Hanlon and Messenger, 1988). Functional convergence between coleoids and fish is, according to Packard, a product of selection pressures exerted by fish and marine reptiles beginning in the Mesozoic. Packard suggested that the radiations of fish and reptiles in nearshore waters drove the externally-shelled (ectocochleate) cephalopods into offshore, deeper habitats in the face of predation and competition. "[R]eduction and even- tually complete loss of the chambered shell ... was an evolutionary response to the needs of increased mobility and to the need to go deeper as vertebrate predators and competitors pushed out into oceanic waters" (Packard, 1972). The coleoids later returned to epipelagic and neritic habitats, where today they compete with, prey on, and are preyed on by teleosts. Vermeij (1987: 270-271) echoed these ideas, though in a less teleological way: "Increasing expression of armor charac- terized many cephalopod lineages during the Paleozoic and Mesozoic, but during the Late Cretaceous predation and competition may have become so intense that the adaptational conflicts resulting from the demands of armor, locomotion, and pressure compensation could no longer be reconciled in a body plan that retained the primitive external shell." O'Dor and Webber (1986) refined Packard's hypothesis. They argued that squid are energetically less efficient than fish due to phylogenetic design constraints. They interpreted rapid growth and semelparous reproduction in squid as responses to selection pressure for predator avoidance (rapid growth because larger squid are less vulnerable; semelparity is then a viable strategy because rapid growth reduces juvenile mortality; see Calow, 1987) and energetic efficiency (rapid growth and early reproduction because smaller squid are more efficient swimmers). Octopuses also "live fast and die young." The spectacular growth rates measured for octopuses (Wells, 1978; Forsythe and Van Heukelem, 1987) may again reduce juvenile mortality, with semelparity then having adaptive value. On the other hand, Boyle (1987) interpreted the coleoid life history as a response to unpre- dictable resources. In fact, octopod life history strategies may be plesiomorphic- a limitation of membership in the coleoid clade having positive, negative, or no adaptive value in modern communities. As we shall see, octopuses are also subject to constraints which arise from some of the very features that help them escape predatory teleosts. Packard (1972, 1988) viewed "competition" between vertebrates and cepha- lopods as a primary driving force in coleoid evolution. He used the term "com- petition" to denote all types of negative biotic interactions, including predation and what ecologists generally call competition. There is at present no direct ev- idence that teleost-coleoid or teleost-Nautilus competition (sensu stricto) is im- portant in modern marine communities (but see Bas [1979] for circumstantial evidence). The possibility of detecting such competition in the fossil record is rather remote. By contrast, predation and its evolutionary consequences for ec- ARONSON: ocroPus EVOLUTION AND ECOLOGY 247 tocochleates are recorded in ancient sediments. And, as discussed in the next section, predation has an extremely important influence on the ecology of coleoids in modem benthic communities. I think it most fruitful, therefore, to concentrate on the ethological, ecological and evolutionary consequences of predation, and to table the issue of competition pending further evidence. Predation, as it hap- pens, explains a great deal. If the decline of the ectocochleates was mediated by predation, then that decline was one of many effects of a general, large-scale predation increase in shallow- water environments during the Mesozoic. Modem predators-teleostean fishes, neoselachian sharks, and decapod crustaceans-radiated explosively in the Me- sozoic (Vermeij, 1987; Reif, 1988). From the Jurassic onward, increasing duropha- gous (skeleton-crushing) predation by fish and crustaceans (as well as by some marine reptiles) was associated with an evolutionary increase in the defensive architecture of calcareous red algae (Steneck, 1983), gastropods (Vermeij, 1977; 1983), crinoids (Meyer and Macurda, 1977) and ammonites (Ward, 1981). In- dividual clades of epifaunal suspension-feeders, and the communities they com- prised, were largely driven out of shallow, soft-substratum habitats (Meyer and Macurda, 1977; Stanley, 1977; Aronson and Sues, 1987; Bottjer and Jablonski, 1988; Aronson, 1989a). Vermeij (1977) named this biotic upheaval the "Mesozoic marine revolution." The history of the crinoids, as elucidated by Meyer and Macurda (1977) and Bottjer and Jablonski (1988), is particularly illuminating when it comes to rec- onciling Packard's ideas with the stratigraphic distribution of the coleoids. Stalked and un stalked (comatulid) crinoids inhabited both shallow- and deep-water en- vironments in the early Mesozoic. Predators in shallow habitats apparently elim- inated stalked crinoids by the Middle Cretaceous, and today they rarely occur above 100 m depth (Meyer and Macurda, 1977; Oji, 1985). The comatulids,
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