Hearts and minds

Not only do certain invertebrates provide some intriguing parallels to the behavioural sophistications of the vertebrates, but they also approach them in terms of activity and intelligence. Earlier I emphasized the convergent similarities between the camera-eyes of cephalopods and vertebrates (p. 151).101 In addition, despite the rather different arrangement of the cephalopod brain,102 the size of this organ relative to the body exceeds that of many fish and reptiles.103 In addition, in at least the cuttlefish, the blood-brain barrier,104 essential for controlling the chemistry of the brain and thereby a prerequisite for high level integration, 'is as tight as that of mammals'.105 The cephalopods also appear to share another characteristic, the possession of molecules similar to those known in vertebrates as neurotrophins, a type of protein growth factor. This, as has been suggested, may be a prerequisite for the emergence of complex brains.106 Cephalopods are fascinating animals and, notably in the cuttlefish, they can show an astonishing range of chromatic signals that are under direct nervous control. To see the colours flowing across a cuttlefish is a quite extraordinary sight, and although the colour changes are well attested with respect to camouflage and predator avoidance, it is difficult to believe that it is not in some way 'emotional'.107 In the case of the octopus, there is an intelligence that includes a flexibility in behavioural repertoires and the ability to learn and remember.108 Evidently the octopus, far from being a rule-bound machine, is capable of acting in an autonomous fashion.109 In their natural habitat octopuses have a sound grasp of the seascape: as one report110 commented, the octopuses 'often zigzagged through multiple substrata and depths, with many obstacles obscuring their visibility of the horizon. The divers [who were tracking them] were often surprised when a forage ended and they realized the octopus had arrived back at its den while the divers themselves were still disoriented.'111 Some workers have gone so far as to talk about the individual temperament, if not personalities, of the octopus.112

Given these characteristics, it is scarcely surprising that the octopus and the squid are very active animals, with maximal power outbursts that compare favourably with those of human athletes. This type of activity presupposes an effective circulatory system. As such it finds strong parallels to ourselves in two ways: the structure of the aorta and the pattern of circulation. Although rather different, both are related to the necessity of supplying oxygen at a fast enough rate. In such circumstances high blood pressures are essential. Blood leaves the heart via the arteries, and to deal with the repeated fluctuations in pressure it is hardly surprising that the arterial walls are rich in specific proteins that confer an elasticity to the throbbing tube.113 Nor is it really surprising that the structure of the aorta wall in squid and human is strongly convergent.114 The other parallel concerns the general arrangement of the circulatory system. Elevated blood pressure is essential for an active (and intelligent) animal, but if directed to the respiratory organs (lungs or gills) there is a danger that it will rupture the delicate membranes across which the gases are exchanged. The solution is simple and to some extent convergent. Only in the cephalopods115 and vertebrates is the circulatory system completely enclosed in vessels and so capable of operating at high blood pressures. In both there is effectively a dual system, whereby the blood is first pumped to the lung/gill in order to collect the oxygen (and dispose of carbon dioxide). The blood is then returned to a second set of chambers in the heart where it is dispatched at full force into these elastic arteries. Even so, despite the shared principle there are significant differences. The branchial heart in cephalopods, which as the name indicates is responsible for feeding blood to the gills, is separate from the main pump. Furthermore, it is not very muscular, and probably has additional excretory functions.116 The main systematic heart is powerful and muscular, but its structure only approximates to the vertebrate arrangement.117

Despite their manifest differences, the convergences between the cephalopods and vertebrates have attracted the attention of many biologists. Of greatest significance surely are those that pertain to the camera-like eye (Chapter 7) and brain (note 108). Others are probably less significant, but still intriguing. Earlier, in discussing the hypothetical Fortean bladders I remarked on the convergence between the relatively familiar fish swim-bladder and that of an octopus (note 35, Chapter 6). Another interesting convergence with the vertebrates is the development of a cartilage-like tissue in the head.118 In fact, the roster of convergences is still not complete. Consider, for example, that part of the cephalopod sensory system associated with the skin. This is strongly analogous to the lateral-line system found in the fish and aquatic amphibians,119 and it too is sensitive to pressure waves travelling through the water.120

Having reviewed earlier (Chapter 7) not only convergences in particular sensory systems but also possible underlying commonalities (which are equally important), it is not surprising that, at least so far as the fish are concerned, there is evidence that the lateral line can help the animal to form a 'hydrodynamic image'.121 What sort of 'map' or 'image' this might form in the brain is still a matter for speculation. It is likely, however, that the input from the lateral line produces a 'pressure world', analogous both to the 'electrical world' of the mormyrids and other electrosensitive fish and to one that is integrated with other sensory inputs, such as vision.

Self-evidently, as an aquatic adaptation the lateral line of the fish (and amphibians) was lost as the tetrapods clambered on to land. In the case of the manatees (or dugongs), which are secondarily aquatic mammals, the arrangement and anatomy of the post-cranial hairs are something of an evolutionary novelty. Their sensitivity to changes

figure 8.6 A surprising convergence on the lateral line system of fish and cephalopods, as manifested in the trailing antenna of a penaeid crustacean. The structure defines a tunnel with spaced bunches of sensory hairs, and so is a direct analogue of the pressure-sensitive system of the other two groups. (Reproduced from Pl. 1a of Denton and Gray (1985; citation is in note 123) with the permission of the authors and the Royal Society.)

figure 8.6 A surprising convergence on the lateral line system of fish and cephalopods, as manifested in the trailing antenna of a penaeid crustacean. The structure defines a tunnel with spaced bunches of sensory hairs, and so is a direct analogue of the pressure-sensitive system of the other two groups. (Reproduced from Pl. 1a of Denton and Gray (1985; citation is in note 123) with the permission of the authors and the Royal Society.)

in water pressure, however, offers an intriguing analogy to the lateral line,122 and is consistent both with the poor eyesight of these creatures and with the murky waters they inhabit. Because I regard the convergences among sensory systems as being of particular importance, in the context of lateral lines it is surely necessary to remark on an even more striking example: that between the lateral-line system of the fish and the modified antennae of some swimming crustaceans known as the penaeids.123 These pelagic arthropods have a pair of flagella-like antennae (Fig. 8.6), which project from the head at right angles before bending sharply and trailing parallel to the animal as it swims through the water. As in many other arthropods, the antennae have hair-like setae, but these are recurved and so define a tunnel-like structure on the floor of which are located sensory setae. Despite their quite different origin these antennae function in effectively the same way as the lateral line of a fish; in each case the basic structure is a tube with sensory hairs sensitive to changes in the water pressure.

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