Perception and discrimination as a function of stimulus orientation: The "oblique effect" in man and animals.

Summary
Resemblances between cephalopods and fish

1. Modern cephalopods (coleoids < 1000 species) resemble modern fish (30,000 species) more closely than any of their ancestors did. They have not been replaced by the more diversified group in geological time.

2. The main body of the article (pp. 245–283) reviews these resemblances. They are to be found at all levels of analysis.

3. Basic physiological mechanisms of molluscs (pp. 262–5) have been incorporated into systems with performances comparable to those of vertebrate systems. For instance the cephalopod locomotory system (pp. 249–56) and hydrostatic control system (pp. 256–60), structurally very different from their fish counterparts, have similar adaptive radiation.

4. Behaviour (p. 278) and growth of the brain (p. 265) are characteristically vertebrate-like.

5. Cephalopods and fish are considered as occupying the same broad adaptive zone though modal differences (pp. 283–5)-in reproductive habits, growth rate and light-dependent behaviour where extraocular photoreceptors appear to be important - mean that they occupy different areas within that zone.

(ii) Evolution of convergence

6. Evidence is presented (pp. 287–293) for considering the convergence as due not merely to similar physical demands of the marine environment, but to dynamic interactions between cephalopods and vertebrates from the late Palaeozoic onwards.

7. The convergence was set on its way when the two groups, independently of each other, acquired locomotory methods that allowed them to increase in size.

8. It is argued that reduction and eventually complete loss of the chambered shell (in all but sepiids) was an evolutionary response to the needs of increased mobility and to the need to go deeper as vertebrate predators pushed out into oceanic waters.

9. The ammonites (pp. 291–2) present a partial model of the course that coleoid ancestors may have taken.

10. Coleoids subsequently reinvaded surface and coastal waters, competing successfully in a teleost habitat. Their most striking adaptations are ones that they share with teleosts.

11. Behavioural interactions in a vertebrate-dominated environment have probably been responsible for the vertebrate-type eye of cephalopods (p. 293).

12. The conclusion that the common adaptive zone shared by cephalopods and fish has been achieved by mutual interactions between the two groups evokes no special evolutionary principles. It assumes that all cephalopod species have (at some period of their evolutionary history) been in competition for food with some vertebrate species and that vertebrates are a source of selection pressures - largely operating through visual behaviour - that maintain and promote convergence upon the ‘fish’ modal type.

13. Selection pressures also operate within behaviour space to maintain and promote the special differences that separate any competitively successful species from all others. Coleoids as a group appear to have retained adaptations associated with such molluscan features as high growth rate and rapid turnover of the population. They are still characteristically crepuscular in habits and have extensive vertical mobility.

Cephalopods and fish: the limits of convergence

Preface.Acknowledgements.Introduction.Form and Function.Origin and Evolution.Nautilus: The Survivor.Biodiversity and Zoogeography.Life Cycle.Growth.Physiological Ecology.Reproductive.From Egg to Recruitment.Coastal and Shelf Species.Oceanic and Deep-Sea Species.Cephalopods as Predators.Cephalopods as Prey.Fishing Methods and Scientific Sampling.Fishery Resources.Fisheries Oceanography.Assessment and Management.Conclusions.Appendix A: Classification of Living Cephalopod Families.Appendix B: Synopsis of Living Cephalopod Families.References.Index.

Cephalopods: Ecology and Fisheries

Integrating the effects of multiple stressors and predicting their consequences for the species' survival and distribution is an important problem in ecological physiology. This review applies the concept of energy-limited tolerance to stress to develop bioenergetic markers that can assist in integrating the effects of multiple stressors and distinguishing between the moderate stress compatible with long-term survival of populations and bioenergetically unsustainable extreme stress. These markers reflect the progressive decline of the aerobic scope of an organism (defined as the fraction of the energy flux and metabolic power supporting this flux available after the basal maintenance costs of an organism are met) with increasing levels of the environmental stress. During the exposure to moderate stress (i.e., in the pejus range of the environmental conditions), the aerobic scope is positive but reduced compared with the optimum conditions. The reduction of the metabolic scope can be due to the (1) elevated costs of basal metabolism, (2) activation of the mechanisms for protection and damage repair, (3) reduced assimilation of food, and/or (4) stress-induced impacts on the aerobic pathways producing ATP. This leads to suboptimal growth and reproductive rates in the pejus range of environmental conditions and is commonly observed in food-limited and energy-limited wild populations. The tolerance windows of the organisms are delimited by the pessimum range(s) of environmental conditions in which the aerobic scope of the organism disappears (so that all available energy and metabolic capacity are used in support of basal metabolism), energy resources are depleted, and partial anaerobiosis and/or metabolic rate depression set in. The habitats where environmental conditions remain in the pessimum zone long enough to prevent consistent growth and reproduction often coincide with the species' distributional limits. Thus, focus on the bioenergetic effects of environmental stressors and their immediate consequences for fitness provides a suitable framework for integrating physiology and functional ecology and can assist in understanding the driving forces and limitations of environmental adaptation and improving assessment of ecological risk as well as environmental management in field populations facing multiple stressors.

Energy-Limited Tolerance to Stress as a Conceptual Framework to Integrate the Effects of Multiple Stressors

Publisher Summary This chapter describes the maximum number of common factors in the growth control system of insects; reviews current ideas about the nature of the action of the hormones at the cellular level; and differentiates these immediate effects from the secondary consequences of hormonal action. It is now well recognized that the cell body of the neurons in insects, as in other animals, is in a state of more or less continuous secretory activity. But nerve cells with distinctive secretory activities, as judged by histological coloration, exist in all the nerve ganglia of insects. The action of insect hormones is commonly associated with a rise in oxygen consumption. A single hormone can produce widespread effects on morphogenesis and metabolism. But during normal growth, several growth hormones may be operating, as happens with the brain hormone, thoracic gland hormone, and corpus allatum hormone during larval moults or the brain hormone and corpus allatum hormone during reproduction. In the course of growth and moulting, the cellular processes take place in a regular sequence, which is correlated with changes in metabolism throughout the body. The metabolic change at maturation in Melanoplus is also followed by great increases in nonfatty material (probably glycogen) and water. In recent years, the metabolic effects of hormones in reproduction have been complicated by the discovery of the role played by the neurosecretory cells.

The Hormonal Regulation of Growth and Reproduction in Insects

1. Gonad and body weight records have been collected for 487 individual octopuses over a period of 3 years. 2. In the size range used for experiments (200-1000 g.), the ovary is always immature in control animals, and constitutes only about 1/500th of the total body weight. The testis is rather larger, generally ripe, and forms about 1/100th of the body weight, increasing somewhat relative to the size of the body over the range considered. 3. Following optic nerve section, or removal of certain parts of the supraoesophageal lobes, the gonads enlarge. In females the ovary enlarges from 1/500th to as much as 1/5th of the total body weight within 5 weeks of operation and this may be followed by laying of fertile eggs that are brooded in a normal manner. In males where the testis is generally mature before operation the enlargement produced is only of the order of 50%. 4. Enlargement of testis or ovary is always accompanied by enlargement of one or both of the optic glands, and operational treatments that normally cause enlargement of the gonad are ineffective if the optic glands are first removed. 5. The optic glands are innervated from the subpedunculate/dorsal basal area in the hind part of the supraoesophageal brain mass. Lesions in this area, or severance of the nerve tracts running along the sides of the brain from it to the optic glands, cause these and the gonads to enlarge. 6. Unilateral central lesions or optic nerve section cause optic gland enlargement on the operated side only, but appear to be as effective in determining gonad enlargement as bilateral treatments. 7. It is concluded that maturation of the gonad is determined by secretion from the optic glands which is normally held in check by an inhibitory nerve supply from the subpedunculate/dorsal basal lobe area. The action of this region is in turn dependent upon the integrity of the optic nerves and thus, presumably, upon light. 8. This system in cephalopods is compared with analogous systems regulating sexual maturity in arthropods and vertebrates.

Hormonal control of sexual maturity in octopus

Octopus vulgaris can be forced into precocious maturity by removal of the subpedunculate lobe from the brain, an operation that releases the optic glands from inhibition, and allows them to secrete a gonadotropin. 14 C-leucine was injected into the bloodstream of immature animals and its subsequent incorporation into muscle protein followed by taking successive samples from the arms. The optic glands were then activated, and a further injection of 3 H-leucine given and followed by means of further arm samples. Optic gland secretion suppresses protein synthesis in the muscles. This is associated with an increase in the total amino acid pool in the muscles and with a considerable increase in the concentration of free amino acids circulating in the blood. If an ovary is present these events are associated with a rapid growth of the ovary and its ducts, and a loss of weight elsewhere. In ovariectomized animals the ducts grow, but there is no yolk to absorb the large pool of free amino acids, and the animals gain weight by osmotic uptake of water into the muscles. The developing ovary may produce a hormone that increases the release of amino acids from muscle, since the concentration circulating in the blood of intact animals remains at least as high as in ovariectomized octopuses, despite the demands of the developing ovary. These matters are discussed in relation to other evidence for a gonadial hormone and in relation to the ‘self-destruct’ effect of the optic gland secretion in determining the post-reproductive death of octopuses.

Reproduction Versus Somatic Growth: Hormonal Control in Octopus Vulgaris

Despite the very considerable difficulties presented by the basic molluscan anatomy and the possession of a blood pigment with an oxygen carrying capacity that never exceeds 4.5 vols%, the cephalopod circulatory system contrives to deliver oxygen at a rate fully comparable with that of an active fish. This is achieved by adding accessory pumps to push blood through the gills, by a multiplicity of pulsatile veins and by raising the systemic blood pressure considerably above the levels found in other molluscs. Detailed control of blood distribution is a necessity in a system where the peripheral resistences may be expected to change dramatically when the animal starts to move and large parts of the central nervous system are apparently dedicated to this task. In this account we have reviewed blood pressure and flow at rest and in exercise. We have further examined the evidence which indicates how the animals modulate the cardiac output, drawing attention to the very different response found in cephalopods and the higher vertebrates.

The performance of the octopus circulatory system: A triumph of engineering over design

1. Twenty-two small octopuses were trained to make visual discriminations before and after removal of the statocysts. 2. Removal of one statocyst (left or right) did not affect performance in a visual discrimination of rectangles shown horizontally and vertically (8 experiments), nor did it determine which eye was used to guide attacks upon things seen (a record of this was kept in four of the experiments). 3. Removal of both statocysts did not affect performance in a discrimination between black and white circles (7 animals) but did destroy the capacity to discriminate successfully between rectangles shown horizontally and vertically (11 animals). 4. After removal of both statocysts the orientation of the retina (as indicated by the slit-like pupils) is no longer constant over the normal wide range of bodily positions, but depends upon how the animal is sitting on the side or bottom of its tank. 5. An analysis of the postoperational responses of animals trained to make the orientation discrimination showed that nearly all of them were biased in favour of one or other of the test figures, not always that used as ‘positive’ figure during preoperational training. The postoperational scores of these trained animals depended mainly upon the positions in which they habitually sat in their tanks; ndividuals in positions such that the retina of the eye used to observe the test figures lay at right angles to the position held during pretraining tended to behave perversely. 6. These results indicate that orientation discrimination is dependent upon correct orientation of the retina, rather than upon central integration of proprioceptive and visual information. This is discussed in relation to a possible mechanism of visual discrimination proposed by Sutherland (1957), and in relation to what is already known about the role of proprioceptive information in learning.

Proprioception and Visual Discrimination of Orientation in Octopus

1. Octopuses will make detours to get at prey seen through a transparent barrier, even though the detours carry them temporarily out of sight of the prey. The possibility of non-visual intermediate cues can be eliminated experimentally. 2. Eight out of 29 octopuses tested made a successful detour at the first trial. The remainder had to be led through the maze by means of a crab on a string on one or more occasions before they did it spontaneously. 3. Once having completed a successful detour down a passage to get into a feeding compartment to the side of the corridor, an octopus rarely failed in subsequent trials, whether making a detour to right or to left. Eleven unoperated control animals, each tested 20 times, totalled only 10 errors, by going into the feeding compartment on the wrong side of the corridor; they failed to make a detour only 13 times in 220 trials. 4. Performance nevertheless showed some improvement with practice. The number of seconds spent attacking through the wall of the feeding compartment before entering the corridor and the number of abortive entries into the corridor both decreased as trials continued. 5. Removal of the statocysts did not stop the high proportion of correct responses. In 39 trials four animals made 6 errors, 3 of them attributable to unilateral blinding of one of the animals (see below). 6. Blinding the animals in one eye led to systematic errors in detours towards the unblinded side. In 63 trials towards the unblinded side, four octopuses made 16 errors and failed to complete the detour 28 times. In 63 trials towards the blind side there were only 4 errors and 9 failures. 7. It is concluded that orientation in detours is maintained by keeping close visual contact with the wall separating the octopus from its prey. The experimental results indicate that octopuses do not take bodily position into account in learning to make detours. 8. Animals trained to make a detour to one side only performed faultlessly when first required to make a detour in the other direction; there is no indication that octopuses are guided by external cues in these experiments. 9. These results are discussed in relation to the organization of motor and learning systems in animals generally. Creatures with hydrostatic skeletons and flexible bodies must of necessity have a decentralized motor control system, and this has important consequences on their learned behaviour.

M. J. Wells

Papers

Hormonal control of sexual maturity in octopus

Reproduction Versus Somatic Growth: Hormonal Control in Octopus Vulgaris

The performance of the octopus circulatory system: A triumph of engineering over design

Proprioception and Visual Discrimination of Orientation in Octopus

Detour experiments with octopuses