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The History of every major Galactic Civilization tends to pass through three distinct and recognizable phases … the first phase is characterized by the question How can we eat? the second by the question Why do we eat? and the third by the question Where shall we have lunch?
Douglas Adams, The Hitchhiker's Guide to the Galaxy
INTRODUCTION
Ecological hypotheses for the evolution of great ape intelligence relate selective pressures for increased intelligence to biological and environmental parameters such as body size, metabolic rate, life history, diet, home range size, habitat stratification, and predation risk (Clutton-Brock & Harvey 1980; Dunbar 1992; Gibson 1986; Milton 1981, 1988; Sawaguchi 1989, 1992). Of these, diet is the ecological selective pressure most frequently invoked to explain the emergence of great ape cognitive abilities. A correlation between diet and relative brain size in primates has long been established; frugivorous primates tend to have relatively larger brains than closely related folivorous taxa (Clutton-Brock & Harvey 1980; Milton 1981, 1988; Sawaguchi 1992). This pattern was most often explained in terms of the differing nutritional properties of fruits and leaves. A high-energy, fruit-based diet, it was thought, released energetic and metabolic constraints, allowing accelerated neonatal brain growth and maintenance of relatively greater adult brain mass (Jolly 1988; Martin 1981). However, the expansion of energy-hungry brain tissue will occur only where it confers an immediate adaptive advantage (Dunbar 1992). In other words, adequate energy supply is a necessary precondition for, but not in itself a sufficient stimulus to, increased encephalization.
Researchers seeking such a stimulus have tended to focus upon the adaptive role of intelligence in solving the unique foraging problems posed by primate diets.
Research increasingly shows great apes surpassing other nonhuman primates in their mentality, achieving abilities traditionally considered uniquely human. Importantly, the cognitive capacities that distinguish them include rudimentary symbolic processes, in the sense of processes that operate on the basis of mental images rather than direct sensory-motor phenomena. Although this view does not represent consensus among experts (e.g., Tomasello & Call 1997), many well-respected researchers now accept this interpretation of the empirical evidence (e.g., Byrne 1995; Langer & Killen 1998; Parker & McKinney 1999; Parker, Mitchell & Boccia 1994; Parker, Mitchell & Miles 1999; Russon, Bard & Parker 1996; Savage–Rumbaugh, Shanker & Taylor 1998; Whiten & Byrne 1991; Wrangham et al. 1994).
If great apes are capable of symbolic cognitive processes, views of symbolism as having evolved within the human lineage are incorrect. Implications for understanding cognitive evolution within the primates are complex and important. First, neither the landmark significance of symbolism to cognition nor its importance in understanding the evolution of higher primate cognition is diminished by this revision. What is altered is timing. Symbolic cognition shifts from an achievement of the human lineage to a foundation for it. Second, reconstructions of the conditions leading to the evolution of symbolic processes remain important, but existing reconstructions lose much of their weight because they focus on conditions linked with the divergence of the human lineage. If symbolic processes are the joint province of humans and great apes, ancestral large hominoids are their probable evolutionary source.
This book arose from three realizations. First, there is an important need for good models of great ape cognitive evolution. Studies of comparative primate cognition over the last two decades increasingly show that all great apes share a grade of cognition distinct from that of other nonhuman primates. Their cognition appears to be intermediate in complexity between that of other nonhuman primates and humans, so it offers the best available model of the cognitive platform from which human cognition evolved. Understanding the position of the great apes is then essential to understanding cognitive evolution within the primate order and ultimately, in humans. Second, existing reconstructions of the evolutionary origins of great ape cognition are all in need of revision because of advances in research on great ape cognition itself, on modern great ape adaptation, and on fossil hominoids. Third, developing an accurate picture of the evolutionary origins of great ape intelligence requires bringing together expertise from a highly diverse range of fields beyond modern great ape cognition. Essential are current understandings of the brain, life histories, social and ecological challenges, and the interactions among them in both living and ancestral hominids.
We therefore assembled a team of contributors with expertise spanning the topics currently recognized as relevant to cognitive evolution in the great ape lineage, with the aim of piecing together the most comprehensive picture possible today. We asked all our contributors to explore the implications of their realm of expertise for cognition and cognitive evolution.
Helping behavior is enigmatic as it appears to entail an individual sacrificing personal reproduction while assisting others in their breeding attempts. Over the past 40 years, the field of cooperative breeding has developed a rich body of theory to explain helping behavior, and enough cooperative species have been studied in detail to establish common ground and test theory. Indeed Emlen (1997a) stated that the original paradox of cooperative breeding had largely been resolved with the widespread confirmation that (1) helpers are often individuals that are constrained from breeding due to a shortage of quality breeding opportunities, (2) helpers unable to obtain breeding positions in the current year frequently improve their chances of becoming breeders in the future, and (3) helpers frequently obtain large indirect benefits by helping to rear collateral kin. With identification of these direct and indirect benefits to helpers, Emlen suggested that the original questions asked by researchers in this field would appear to be “largely answered.”
In contrast, Cockburn (1998) concluded that “we are still some way from understanding the adaptive significance of helping behavior although we are poised for a reinvigoration of the study of cooperation through a number of conceptual, empirical, and technical advances.” Clearly, conceptual breakthroughs have been made, but many important questions also remain unanswered. In particular, our understanding of the varying level of helper contributions within and between species and how these contributions benefit breeders and helpers remains poor.
DOES GREAT APE INTELLIGENCE DIFFER FROM THAT OF MONKEYS?
There is growing consensus that great apes' intellectual abilities are qualitatively distinct from those of other primate taxa, as seen in their mirror self-recognition (e.g., Gallup, 1970) causal understanding of tool-using tasks without trial and error (Visalberghi, Fragaszy & Savage-Rumbaugh 1995), and imitative ability (e.g., Custance, Whiten & Bard 1995), among other traits and abilities (see Russon, Bard & Parker 1996; other chapters this volume). This raises the important question: In what ecological and social environments did this distinct intellectual capacity evolve?
Potential answers have been much discussed in recent years. Using brain parameters (e.g., absolute or relative brain size, neocortex ratio) as proxies for the rather amorphous concept of “intelligence,” comparative studies (Dunbar 1992, 1995) have found that the size of the social network (represented by group size) better explains variation in the neocortex ratio among primate taxa than any of the ecological parameters considered thus far, such as degree of frugivory, range size, or presence/absence of “extractive foraging.” This suggests that the social complexity resulting from primate-style group living is more likely to be behind variations in primate intelligence, as the so-called “social intellect hypothesis” sets out (Chance & Mead 1953; Humphrey 1976), than the ecological complexity arising from foraging problems, as some others have suggested (Menzel 1997; Milton 1981; Parker & Gibson 1979).
Small vagile epiphytic crustaceans formed the greatest proportion of the diet of worm pipefish. There were significant differences in the number (Mann–Whitney U=22006·5, P<0·001) and diversity (Mann–Whitney U=11546·0, P<0·05) of prey consumed by male and female pipefish. Harpacticoid copepods are the most numerically dominant form of prey consumed. Further gender analysis of mature pipefish revealed that reproductively mature females and egg-bearing male worm pipefish show significantly greater predatory effort (Kruskal–Wallis H=24·15, df=2, P<0·001). Increased feeding activity, within these groups, is suggested to alleviate the substantial reproductive costs for both female and egg-bearing male pipefish.
The spread of the oil spill from the tanker ‘Prestige’ was analysed in relation to the occurrence of the exceptional 2002/2003 Navidad using airborne and AVHRR satellite measurements. Altimeter-derived geostrophic velocity and Envisat ASAR observations were also used to investigate the structure of this Cantabrian extension of the poleward current around Iberia.
The age of the sea urchin Hemicentrotus pulcherrimus in Oshoro Bay at the northern distributional limit of the species was ascertained by counting black bands in charred genital plates after etching. Consequently, the seasonal growth of two year-classes was monitored and the seasonal changes were related to the reproductive cycle and water temperature. A black band at the edge of the genital plates was found in more than 50% of the sea urchins from September to November. No statistical difference of the test diameter and body weight forming the bands between the estimated and actual values showed that the band is formed annually and can be used as a chronometer. The sea urchin grew rapidly for one and a half months, from late August to late September or early October when water temperature reached a maximum of >20°C, then began to fall while the gonads increased in size prior to maturation. Growth ceased during October to November with initiation of gonadal maturation and the peak of black band formation in genital plates. Spawning occurred from March to May, later than in southern Japan. The annual cycle of growth and reproduction of H. pulcherrimus may be flexibly adapted to surbarctic waters.
Two inshore rocky subtidal sites on the west coast of Scotland (Saulmore Point, Firth of Lorn, 056°27′N 005°24′W and Davy's Rock, Firth of Clyde, 055°46′N 004°53′W) were surveyed for the presence of juvenile (0+) Atlantic cod, Gadus morhua between September 1995 and November 2001. A total of 951 juveniles were recorded at Saulmore Point and 34 at Davy's Rock. At Saulmore Point the abundance was highly seasonal, being observed between June and December only. Juveniles were present in only three out of six survey years, with a maximum abundance of 0·89 individuals m−2 recorded in 1996. Maximum abundance of juveniles at Saulmore Point was negatively correlated with winter seawater temperature, indicating that winter temperatures may be a useful indicator of subsequent juvenile abundance levels in inshore habitats.
The predatory effects of Pachygrapsus marmoratus on populations of the intertidal limpet Patella depressa were analysed on rocky shores located on the central coast of Portugal. Nocturnal observations on crab feeding behaviour were conducted and experimental exclusion cages were set in the substratum to assess density effects on limpets. The results indicated that although crabs feed on adult limpets the predatory level was minimal. Crabs used consistent tactics to detach limpets from the substratum but the majority of the attacks were unsuccessful, possibly due to morphological and behavioural adaptations of limpets. An alternative recruitment hypothesis is advanced to explain non-significant differences between experimental treatments and a possible predatory role on shaping levels of recruitment on lower levels of the shore is considered.
Sex ratio and size–gender distribution of Coralliophila meyendorffii and Babelomurex cariniferus collected in the field was studied. While sex ratio did not depart from the expected Fisher 1:1 ratio for dioecious species, the size–frequency distributions showed clearly a sexual size dimorphism with males significantly smaller than females. Laboratory monitoring of penis reduction in both species, combined with an anatomical and histological study of the reproductive system of individuals reducing penis revealed the existence of transitional sexual stages, proving the existence of protandry. Penis monitoring also demonstrated a high plasticity in size at sex change, suggesting a socially controlled sex change. In C. meyendorffii, where penis monitoring followed an experimental design based on the assumption that protandry existed and that presence of females influenced sex change, results strongly supported a social control of sex change. Evidences for protandry in other coralliophilids are summarized and protandry as a widespread sexual strategy in Coralliophilidae is postulated.
The long term effects of macroalgal canopy removal on community composition were investigated over a 12 year period. Experimental removal of the dominant Ascophyllum nodosum canopy led to short term changes in community composition, the major features of which were still apparent 12 years later. Ascophyllum was slow to recover despite high recruitment, and experimental plots were dominated by Fucus species. After 12 years a mixed assemblage of Fucus serratus, Fucus vesiculosus and Ascophyllum had developed. Canopy removal resulted in a change in the balance between grazing limpets and the cover of red algal turf in the understorey community. The cover of turfing algae declined significantly allowing the area grazed by limpets to extend. This led to a 3–6 fold increase in the limpet population 12 years after canopy removal.
This paper describes a study of the ranging and diving behaviour of two ‘offshore’ bottlenose dolphins, Tursiops sp., in the waters off south-east Queensland, determined using satellite-linked time-depth recorders attached to two animals. Animal 1's tag transmitted for 30 days, Animal 2's for 143 days. Immediately after tagging, Animal 1 swam south, reaching a point 146 km south of the point of tagging, then swam generally northwards until the tag ceased working. Animal 2's observed range covered 778 km2, with a core area of 86 km2. The greatest north–south distance between all locations for Animal 2 was 43 km. The manner in which maximum dive depth was related to dive duration was analysed using constrained principal curves. These analyses indicated that for both animals, short dives were to less than 5 m, and there was no clear relationship between dives of greater duration and depth. These dolphins appear to behave differently from ‘offshore’ bottlenose dolphins studied elsewhere.
The diversity and structure of meiobenthic nematodes and macrobenthic infauna were studied at four widely spaced subtidal sites around the UK coast in relation to a number of measured environmental variables. The stations were situated on soft sediments at water depths of 53 to 95 m and are intended as long-term monitoring locations as part of the UK National Marine Monitoring Programme. Similar benthic assemblages were encountered in comparable environmental conditions. The distribution of nematode and macrofauna species was mainly governed by the geographical location of the habitat and the granulometric composition of the substrate. There was no evidence of any adverse effect on the measures of benthic assemblage structure arising from trace metal concentrations in the sediment, indicating the relatively unpolluted nature of the offshore locations under investigation. Nematode and macrofauna assemblages exhibited stable patterns over time periods of three years.
Multiple locus allozyme heterozygosity has been shown to be weakly, but significantly correlated with certain fitness parameters in bivalves. Immune function of individual Mytilus edulis from the Menai Strait, Wales, UK was assessed monthly over one year (1997–1998) by measuring total blood cell (haemocyte) counts, differential haemocyte counts (% basophils and eosinophils), phagocytic capability (by zymozan uptake) and intracellular superoxide generation. Sampled mussels were also scored at 9 allozyme loci. Mussels were then grouped into multiple locus heterozygosity (MLH) classes and plotted separately against the different measures of immunocompetence. No significant association was present between MLH and total haemocyte count, phagocytic capability or intracellular superoxide generation. However, there was a significant association between MLH and the character (basophilic or eosinophilic) of circulating haemocytes (r2=0·057, P=0·002). Highly heterozygous individuals tended to have significantly more eosinophilic haemocytes circulating in the blood than highly homozygous individuals. Eosinophilic haemocytes are known to have a high capacity for phagocytosis of invading organisms and these results may therefore be interpreted as increased health (=fitness) in more highly heterozygous individuals.
The reproductive cycle of a local population the aspidochirote Holothuria tubulosa in Kaštela Bay (Adriatic Sea) was analysed from July 1994 to August 1995 by histological examination and observations of macroscopic features of the gonads. Five gonadal stages were described: recovery stage, growing stage, mature stage, spawning stage, and post-spawning stage. The distinguishing features used to describe gonad stages in both sexes included the main features of reproductive cells and gonad wall. The reproductive cycle showed a clear annual pattern and was synchronous in both sexes. Spawning occurred during the warm season, from July to September, when the surface water temperature ranged from about 22°C to 26°C. From October to January individuals were in resting phase and had no gonads. In both sexes, variations in maturity indices were related to the seasonal changes in temperature.
The diet of Haliclystus auricula was studied from the gut contents of Stauromedusae collected every two months in southern Chile between November 2001 and November 2002. A total of 3790 medusae were collected and examined. Stauromedusae prey consisted primarily of harpacticoid copepods (68·4%), followed by gammarid amphipods (15·4%), chironomid fly larvae (9·2%) and podocopid ostracods (5·9%). The remaining 1·1% of the diet was made up of empidid fly larvae, polychaete worms, isopods, juvenile decapod crustaceans and gastropods. Gut content was observed in 31% of the stauromedusae collected and only in medusae with an umbrella height greater than 0·4 mm. Frequency of medusae with prey items in their gut content increased with stauromedusae size. The type of prey most frequently found in the smallest medusae were copepods, whilst larger individuals contained mainly amphipods. A strong tendency for the length of prey consumed to increase with medusae size was found.
Vertical posture has been studied only in the scutellid sand dollar Dendraster excentricus although it has been reported in another Dendraster species and two species of laganid sand-dollars. The vertical posture has been associated with the posterior eccentric position of the apical system and petals of the test. We have discovered the scutellid sand dollar Encope michelini, which shows no eccentricity of the apical system and petals, also has the vertical posture in the population studied. Absence of eccentricity of the apical system and petals in living and fossil sand-dollars does not indicate absence of the vertical posture.
The morphogenesis and cytogenesis of the salt gland was studied in various embryonic stages of the viviparous Oman shark, Iago omanensis, from the Gulf of Aqaba, Red Sea. The primordium of the gland is revealed in embryos of 18 mm total length (TL) as a protrusion of the gut posterior to the spiral valve, enveloped in the peritoneal epithelium. In 30 mm TL embryos the glandular parenchyma begins to be organized into secretory tubules extending radially and opening into the central canal of the gland. From this stage on the developments include: thickening of the gland capsule and formation of internal lobules by extensions of connective tissue; strong amplification of the basolateral cell membranes of secretory cells into the cell-cytosols; enlargement of the gland by hypertrophy and hyperplasia of the ion-transporting cells. In 65 (±5) mm TL embryos the gland closely resembles that in adult fish and in pre-term juveniles of 165 (±5) mm TL the gland in general morphology and cytology is identical to that of adults. The results demonstrate that at time of liberation into the environment the juvenile of Iago omanensis is provided for osmoregulation with a functional gland.