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 paleontological 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 communities. 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 constraints 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 competition 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 questions, 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 communities, 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 circulatory 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 "fishlike" the coleoids are. Like many teleosts, coleoids are fast-moving, visual predators. They use complex behavioral repertoires in prey capture, predator avoidance, 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 cephalopods as a primary driving force in coleoid evolution. He used the term "competition" to denote all types of negative biotic interactions, including predation and what ecologists generally call competition. There is at present no direct evidence that teleost-coleoid or teleost-Nautilus competition (sensu stricto) is important 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 durophagous (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 environments in the early Mesozoic. Predators in shallow habitats apparently eliminated stalked crinoids by the Middle Cretaceous, and today they rarely occur above 100 m depth (Meyer and Macurda, 1977; Oji, 1985). The comatulids, by virtue of their mobility and antipredator morphology, radiated in shallow habitats. They persist even in high-predation coral reef communities. Our understanding of coleoid evolution is severely hampered by the poor pres- ervation potential of species with reduced internal shells (see Engeser and Bandel [1988] for an attempt at cladistic analysis of the Subclass Coleoidea). Even so, recent paleontological discoveries call into question much of Packard's theory. Coleoids date back at least to the Early Devonian, as Sturmer and colleagues discovered in radiographic studies of the deep-water Hunsruck Shale in Germany (Bandel et aI., 1983; Sturmer, 1985; Engeser and Bandel, 1988). The Mesozoic marine revolution, therefore, cannot account for the evolution of the "advanced" adaptations (streamlined body, reduced internal shell, lens eye) seen in these early fossils. On the other hand, the Devonian coleoids in no way falsify the hypothesis that predatory fish and marine reptiles strongly influenced the later course of cephalopod evolution. By analogy with the case of crinoids, both coleoids and ectocochleates probably inhabited both shallow, onshore and deeper, offshore habitats in the Paleozoic and early Mesozoic. Data on ammonoid stratigraphic ranges suggest that deep- water genera were more extinction-resistant in the Jurassic and Cretaceous (Ward and Signor, 1983). New, predatory teleosts and chondrichthyans may well have played a part in eliminating ectocochleates from shallow water as the Mesozoic came to a close. The coleoids apparently persisted in shallow water, under heavy predation pressure from vertebrates, by virtue of their antipredator adaptations or preadaptations (Fig. 1). Presumably they radiated into at least some of the niches vacated by the ectocochleates. Therefore, we might expect modem nearshore coleoid populations to be strongly influenced by teleostean predators. 248 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

, .'...... 'MODiFiED'.sCENA'RIO

Figure 1. Comparison of Packard's (1972) scenario for the origin of the coleoids with the modified scenario presented in this paper. (A) Packard envisioned the ectocochleates being pushed into ever deeper water by competitors and predators in the Mesozoic. Loss of the external shell was an evolutionary response to the depth limit imposed by hydrostatic pressure. The shell-less, fishlike coleoids subsequently reinvaded shallow water. (B) In the modified scenario, both ectocochleates and coleoids inhabited shallow and deep environments in the Paleozoic and early Mesozoic. Predators and physical events subsequently eliminated ectocochleates from shallow water.

Triggerfish (Balistidae) and groupers (Serranidae) attacked living Nautilus when the Nautilus were released in shallow reef habitats during the day (Saunders et aI., 1987). Saunders (1984; Saunders et aI., 1987) suggested that Nautilus migrate into shallow water only at night to avoid predatory teleosts. Up to 50% of the individuals in populations censused by Saunders et a1. (1987) had repaired shell cracks attributable to tele-ostean predation, although there was a great deal of ARONSON: OCTOPUS EVOLUTION AND ECOLOGY 249 variation among populations in the frequency of damage (Ward, 1987). Sublethal shell breakage due to fishes was considerably less frequent than 50 percent in an assemblage of Mississippian ammonoids, possibly indicating lower predation levels (Bond and Saunders, 1989). However, conclusions regarding predation levels should be deferred until ammonoid injury frequencies are available for other fossil assemblages (also, see Schoener [1979] on the difficulties of interpreting sublethal damage data). The broadscale biotic changes wrought by new, durophagous predators since the Jurassic transcended the end-Cretaceous mass extinction and the extinction events of the Cenozoic (Vermeij, 1977; Aronson, 1989a). Yet the Mesozoic marine revolution was causally connected to another major event in Earth's history: the Permo- Triassic extinctions. The end-Permian extinction paved the way for the evolution of modem predators, and of modem communities in general, by im- poverishing and effectively resetting the marine biosphere (Sepkoski, 1981; Sep- koski and Miller, 1985; Vermeij, 1987; Copper, 1988; reviewed in Aronson and Sues, 1987). Precisely how increasing predation combined with Cretaceous cli- matic change, sea level fluctuations, anoxia, and the end-Cretaceous "event(s)" to eliminate all the ammonoids and more than half the nautiloid genera (Ward, 1981; 1983; Alvarez et aI., 1984; Teichert and Matsumoto, 1987; Weidmann, 1988; Hallam, 1989; House, 1989) remains unknown. Coleoids are the predominant post-Mesozoic cephalopods in part because of increased predation: this much of the original scenario remains intact. Yet the highly predaceous coleoids were themselves Mesozoic "marine revolutionaries." While nautiloid jaws specialized for crushing appeared in the Triassic, it was only after the Jurassic that drilling by octopods and gastropods became a significant form of duro ph agous predation (Vermeij, 1977; 1987; Nixon, 1988). Judging from the frequency of boreholes, octopuses may be important predators of living Nau- tilus (Saunders et aI., 1987). To end this section, it is worth noting that Packard's ideas on the origin of the coleoids may be wrong only in their proposed timing. The coleoid functional grade, which first appears in Devonian sediments, may have evolved in response to an earlier increase in durophagous predation. That predation increase, coin- cidentally enough, took place in the Devonian. Placoderm and primitive chon- drichthyan fishes radiated in the Devonian, and their diversification was associated with an increase in the defensive architecture of nautiloids, as well as other invertebrate groups (Signor and Brett, 1984).

THE OCTOPUS IN MODERN BENTHIC COMMUNITIES Octopuses are notoriously difficult to study in the field (Aronson, 1986; 1989b for reviews of Octopus field studies). Although we now have the paleobiological prediction that modem octopus abundance and distribution should be at least partially controlled by predation, few ecological studies have addressed the predation hypothesis. How do octopuses fit into shallow benthic communities? Octopuses are significant predators of mollusks and crustaceans in some temperate food webs, and fish are their principal predators in those communities (Fotheringham, 1974; Simenstad et aI., 1978; Schmitt, 1982; Ambrose and Nelson, 1983; Fawcett, 1984; Ambrose, 1984; 1988; Hartwick et aI., 1988). Octopus and Eledone can be abundant in intertidal and subtidal habitats in the temperate zone and the subtropics (Mather, 1982; Fawcett, 1984; Boyle, 1986; Ambrose, 1988; Hartwick et aI., 1988). In contrast, octopuses playa minor role in west Atlantic coral reef communities, 250 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991 due to their low abundance (Aronson, 1989b). Predation by nurse sharks (Orecto- lobidae), moray eels (Muraenidae), groupers (Serranidae), snappers (Lutjanidae), barracudas (Sphyraenidae), and other reef fishes (Randall, 1967) apparently limits Octopus abundance on Caribbean reefs. Sweetings Pond, an isolated saltwater lake on Eleuthera Island, Bahamas contains a large population of Octopus briareus Robson. Octopuses were two orders of magnitude more abundant in Sweetings Pond than off the rocky coast of Eleuthera in 1980-1983. High octopus density in the lake was associated with the virtual absence of predatory reef fishes, sug- gesting a causal connection (Aronson, 1986; 1989b). The fisheries literature provides further evidence that teleosts limit octopus populations. Caddy (1983) and Gulland and Garcia (1984) documented an increase in the catch of Octopus and other coleoids on the Saharan Bank (off West Africa) beginning in the late 1960s. The sharp rise in cephalopod abundance was coincident with an equally sharp decline in sparid and other demersal fish stocks, which had been fished heavily. Bas (1979) suggested that this negative correlation of abundance was due to sparid-Octopus competition, while Caddy (1983) at- tributed the Octopus increase to release from predation by demersal fishes on adult cephalopods. Yet a third possibility is release of cephalopod larvae from predation by spa rids (Gulland and Garcia, 1984). None of these hypotheses can be falsified at this time. Similar inverse relationships between cephalopods and fish have been re:vealed through fishing in the Adriatic, the North Atlantic, and Southeast Asia (Brown et aI., 1976; Pauly, 1979; Giovanardi, 1986; G. Bello, pers. comm.). Lacking external shells, Octopus spp. avoid predation through skin color and texture changes, highly flexible bodies, and, in many species, nocturnal activity patterns. They also live in den cavities for protection. In the absence of predatory teleosts, dens were the limiting resource for the O. briareus population on the soft substratum of Sweetings Pond. Enriching 15-by-15 m areas of Sweetings Pond with artificial dens (15 polyvinyl chloride tubes, 5 cm in diameter and 31 cm long, closed at one end) increased Octopus density in those plots substantially after fifteen days (Fig. 2). In contrast, no octopuses migrated into similar experimental plots on a sand bottom near the rocky shore off the west coast ofEleuthera. Instead, fishes utilized most of the artificial dens in the coastal experiment (Table 1; Aronson, 1986). I performed the same experiment in Lameshur Bay, St. John, United States Virgin Islands, on two sand bottoms near rocky shores. Results were similar to the Eleuthera coast experiment (Table 1). Why might octopuses require dens in Sweetings Pond if there are no predatory fishes present? Sheltering in dens may well be a genetic imperative, but Octopus spp. also require protection from intraspecific predation (Hartwick et aI., 1978; Smale and Buchan:, 1981; Ambrose, 1984; Hanlon and Wolterding, 1989), particularly when they occur at high densities (Aronson, 1986; 1989b). Denning has obvious adaptive value in high-predation coastal communities, but the necessity of refuging constrains population density-at least in Sweetings Pond-when predation pressure is released. Intraspecific territorial aggression does not appear to limit density in Swe:etings Pond (Aronson, 1986). Mather (1982) showed that dens were limiting to a dense population of Octopus joubini Robson in a coastal soft substratum community off Florida. As in Sweet- ings Pond, den enrichment experiments increased local density. Shelter availability also limited a population of Octopus tehuelchus d'Orbigny on a sandy bottom in Argentina (Iribarne, 1990). Mottet (1975) cited an experiment in which thousands of artificial dens were added to an octopus fishing ground in Japan, increasing density over a large area. Dens may also be limiting to Octopus doj1eini ARONSON: OCTOPUS EVOLUTION AND ECOLOGY 251

7 D T=O days 6 ~ ~ T=15 days ::: ~ 5 •••• l:::S ••••• •••• ..t:l 4 ~ ::: 3 ~ ~ C- 2

0 Control Experimental Treatment Figure 2. Mean abundances of Octopus briareus in four den enrichment experiments in Sweetings Pond (1982-1983). Error bars represent standard deviations. Experimental plots were enriched with the artificial dens; control plots were not manipulated. Both were censused at the beginning of the experiments and after 15 days. Control and experimental plots were separated by 100 m in two of the experiments, and by 625 m (they were located on opposite sides of Sweetings Pond) in the other two experiments. Only I of the 60 artificial dens in these experiments was occupied by a fish. See Aronson (1986) for data and statistical analysis.

(Wiilker) on sand and gravel, possibly increasing the risk of predation compared to rocky reefs (Hartwick et al., 1988). Hard substratum habitats have more cavities, which may explain why dens are generally not limiting there (Hartwick et al., 1978; 1984; Ambrose, 1982). Yet it is also true that rocky and coral reefs support higher predatory fish densities than soft substrata. This in itself is a shelter- related effect: reef fish will not forage more than a short distance from their own dens (Aronson, 1989c). Higher predation pressure on octopuses in reef habitats may be partially responsible for dens not being limiting.

RESEARCH DIRECTIONS Cephalopod paleobiology yields predictions about the status of the coleoids in modem benthic communities. A few field studies of Octopus spp. provide tan- talizing hints that the "modified Packard scenario" (Fig. 1) and its ecological implications may be largely correct. This theory, with its accompanying testable hypotheses, can give direction to future research efforts. Several potential avenues of inquiry are briefly described below. 1 Abundance and Predation. - What are the biogeographic variations in octopus abundance, diversity and trophic significance? Are these variations inversely related to predation pressure from fishes? 252 BULLETIN OF MARINE SCIENCE, VOL. 49, NO. 1-2, 1991

Table I, Occupants of artificial dens in enrichment experiments off the Eleuthera coast (Site E-I; 1983) and at two sites in Lameshur Bay, S1. John, U,S,V,I, (sites J-I and J-2; 1985). Proportions sum to > 1.00 when some dens were occupied by both fishes and crabs. Fifteen artificial dens were added to each plot, and N = IS except for Site E-I, IS days (N = 14); and Site J-I, 45 days (N = 10) and 60 days (N = II). Some of the artificial dens disappeared from these plots. There were no octopuses in any of the study plots before the experiments

Proportion of dens occupied by Incubation Sile period (d) Octopuses Fishes Crabs Empty E-I IS 0.00 0.93 0.00 0.07 J-l IS 0.00 0.53 0.20 0.33 30 0.00 0.33 0.13 0.60 45 0.00 0.30 0,20 0.50 60 0.00 0.73 0.36 0.09 J-2 IS 0.00 0.53 0.00 0.47 30 0.00 0.67 0.00 0.33 45 0.00 0.47 0.00 0.53

2 Den Limitation. --Are dens usually limiting in low-predation environments? Ambrose (1982; 1988) reported California rocky subtidal Octopus bimaculatus Verrill densities of the same order as O. briareus densities in Sweetings Pond, yet dens were not limiting. Can predation levels drop so low that dens become limiting even on hard substrata? The rocky intertidal is another place to look for den limitation on hard substrata. There desiccation stress generally restricts octopuses to tide pools at low tide. Will drilling den-sized holes in the intertidal increase octopus predation on mollusks and crustaceans? 3 Larval Ecology, Recruitment and Juvenile Ecology. - We know almost nothing about the mortality schedules of planktonic and post-settlement juvenile octopuses (Vecchione, 1987). To what extent does predation at these stages influence adult population density and, hence, the possibility of den limitation? Ambrose (1988) addressed these questions for his O. bimaculatus population in California. His site at Santa Catalina Island is heavily fished, and neither predation nor (as already mentioned) dens are limiting. Ambrose (1982; 1988) suggested that recruitment and juvenile mortality limit adult density in his population. 4 Oveyfishing. - Long-term experimental fish removals from large areas are logisti- cally intractable, but human exploitation of the marine biosphere isa "natural experiment." Octopus populations increased in at least one overfished area (Cad- dy, 1983): how general is this effect? Human fishing activity typically begins near shore and then spreads to offshore environments, changing benthic communities in the same directional manner (Aronson, 1990). Comparing fished onshore and less disturbed offshore habitats at similar depths would help clarify the teleost- coleoid relationship (Ambrose [1988] for discussion on this point). If intensive fishing is increasing coleoid abundance on a geographic scale, we should recom- mend greater exploitation of nearshore cephalopod stocks, a suggestion that would have delighted Gilbert Voss.

ACKNOWLEDGMENTS

This paper is dedicatedl to the memory of Gilbert L. Voss. I thank R. Ambrose, G. Bello, A. Guerra, B. Hartwick, R. Hanlon, J. Havenhand and A. Packard for discussions on the ecology, evolution and paleobiology of cephalopods, and C. E. Roper for the opportunity to contribute to this volume. P. Boyle, R. Etter, R. Hanlon, R. Mooi, C. Roper and H. Sues commented on earlier versions of the ARONSON: OCTOPUS EVOLUTION AND ECOLOGY 253 manuscript. A 1988 octopus cruise to the Channel Islands of California, organized by M. Lang and J. Engle and financed by the Tatman Foundation, helped me crystallize the ideas presented in this paper. R. Mooi drew Figure 1. Supported by the Smithsonian Scholarly Studies Program.

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DATEACCEPTED: January 9, 1991.

ADDRESS: Department of Invertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington. D.C. 20560.