Notes

MARINE MAMMAL SCIENCE, 13(1):133-138 (January 1997) 0 1997 by the Society for Marine Mammalogy

THE RELATIONSHIP BETWEEN GESTATION LENGTH, ENCEPHALIZATION, AND BODY WEIGHT IN

ODONTOCETES

Using multiple regression techniques, Sacher and Staffeldt (1974) reported that, for a wide range of mammalian species, gestation length (i.e., duration) increases with neonatal brain size and decreases with litter size. Moreover, neonatal brain size is positively correlated with adult encephalization levels in many mammals (Page1 and Harvey 1989). Encephalization is a measure of degree of brain development. It is typically utilized at the level of species or higher taxonomic categories. Encephalization Quotient (EQ) is a measure of encephalization that, essentially, is equivalent to relative brain size accounting for allometric trends in the brain weight-body weight relationship across groups (e.g., species). EQ has been shown to be positively correlated with a number of general measures of cognitive processing ability in different mam- mals (Hodos 1970; Masterton and Skeen 1972; Riddell and Corl 1977; Riddell et al. 1976a,b; see Marino 1995 for a review). EQ and related measures of relative brain size are, in turn, positively correlated to a number of life history patterns in mammals such as dietary strategy (Clutton-Brock and Harvey 1980; Eisenberg and Wilson 1978, 1981; Gibson 1986; Mann et al. 1988), social group size (Dunbar 1993, Sawaguchi and Kudo 1990), and weaning age (Eisenberg 1981). In short, the relationship between neonatal brain size, EQ, and a number of behavioral-ecological factors are consistent with the pattern known as r-K selection identified by MacArthur and Wilson (1967) for terrestrial mammals.

According to the notion of r-K selection, highly K-selected species are characterized by large body mass, delayed maturation and reproduction, few offspring, extended parental care, long life span, large relative brain size, and a high degree of behavioral complexity and flexibility. Among terrestrial mam- mals this dimension is anchored at the K-selected end by the highly ence- phalized primate order. Furthermore, EQ is a good predictor of life history patterns and behavior among primates (Dunbar 1993, Economos 1980, Sa- waguchi and Kudo 1990).

However, the odontocetes, many of which have a higher encephalization level than most primates (Marino 1995), have been largely ignored in studies

133

134 MARINE MAMMAL SCIENCE, VOL. 13, NO. 1, 1997

of consistent patterns in brain size and behavior among mammals. Therefore, the relationship between EQ and a life history factor (gestation length) for which adequate data exists in odontocetes, was examined in odontocetes in an effort to preliminarily address the question of whether odontocetes share pat- terns of relations between brain size, behavior, and life history with terrestrial mammals, particularly the primates.

Data on brain and body masses for fifteen species from five families within the suborder Odontoceti were obtained from the literature and by direct mea- surement of cranial volume of osteological specimens from the National Mu- seum of Natural History at the Smithsonian Institution. Cranial volume was measured by plugging each cranium and filling it, vi& the foramen magnum, with plastic beads to the lower ridge of the foramen magnum. Each skull was then emptied and the volume of beads measured with graduated cylinders. Measurements for a randomly chosen one-half of the specimens were repeated one to three days after the initial measurement. The average reliability of the measurements was 1.34%. For individual species the reliabilities ranged from 0.36% to 2.48% (Marino 1995). Data from juvenile, sick, emaciated, or gravid specimens were excluded. Data for both sexes were combined because a t-test of the difference in mean EQ for the sexes indicated no significant sex differ- ences in EQ (t = 0814, P = 0.42, n = 11). Body weight data for each specimen were taken from collection files. Only data from specimens with a normative adult body weight were included. Normative body weight data were obtained from Ridgway (1972), Leatherwood and Reeves (1983), Bryden (1988), and Read et al. (1993).

EQ values were calculated for each species using log mean brain weights (or cranial volume in the case of those directly measured by the author) and log mean body weights of the specimens. EQ calculation was based on the following formula derived by Jerison (1973) in his regression analysis of log brain weight on log body weight for a wide range of mammals, including dolphins and whales:

EQ = Brain Weight

0.12 (Body Weight)0.67

Therefore, this measure of EQ represents the level of encephalization in each odontocete species relative to most other mammals, i.e., those used in Jerison’s regression analysis. Furthermore, this formula has become a standard by which many authors have previously compared species (Terison 1973, Clutton-Brock and Harvey 1980, Mace et al. 1980).

Mean gestation-length values for the species within the sample were ob- tained from Ridgway (1972), Slijper (1979), Gaskin (1982), Leatherwood and Reeves (1983), Best and da Silva (1989), and Ridgway and Harrison (1.989). When more than one published value for a given species was found, the results were averaged. In no cases were published values markedly discrepant.

Data on EQ, mean gestation length, and mean body weight are displayed in Table 1 for each of the fifteen odontocete species in the present analysis.

NOTES 135

Table 1. EQ, mean gestation length, and mean body weight for the odontocete sample.

Species (number of specimens) EQ

Gesta- tion Body wt

(days) (kg) Source*

Family Delphinidae Tursiops truncatus (20) Globicephala melas (5) Delphinus delphis (6) Sotalia fluviatilis ( 1) Lagenorhynchus obliquidens (4) Orcinus orca (2)

Family Monodontidae Delphinapterus leucas ( 1) Monodon monoceros (3)

Family Phocoenidae Phocoena phocoena (1) Phocoenoides dalli (11)

Family Platanistidae Platanista gangetica (4) Inia geoffrensis (15) Lipotes vexillifer ( 1) Pontoporia blainvillei ( 14)

Family Ziphiidae Ziphius cavirostris (1)

4.14 360 209.53 2.39 435 943.20 4.26 276 60.17 4.56 300 42.24 4.55 365 91.05 2.57 435 1,955.45

2.24 420 636.00 n 1.76 450 1,578.33 C

2.59 315 61.10 i 3.54 365 86.83 i, P

1.55 255 59.63 k 2.51 315 90.83 a, i 2.17 180 82.00 b 1.67 315 34.89 d, f, i

0.92 365 2,273.OO n

e, g, j, 1, m, 0 zj

g g, L P i

* Source of brain weight and body weight data from which mean EQ was calculated for each species. (Note that EQ values for those species from which data was collected by Marino (1995) include values for some specimens for which cranial volume was measured instead of brain weight). Sources: a = Best and da Silva (1989), b = Chen Iyu (1979), c = Hay and Mansfield (19&9), d = Kamiya and Yamasaki (1974), e = Kruger (1959), f = Marino (1995), g = Morgane and Jacobs (1972), h = Pilleri and Busnel (1969), i = Pilleri and Gihr (1968), j = P 11 i eri and Gihr (1970a), k = Pilleri and Gihr (19706), 1 = Ridgway (1986), m = Ridgway and Brownson (1979), n = Ridgway and Brownson (1984), o = Ridgway et al. (1987), p = Ridgway et al. (1966).

An analysis of the correlation between EQ and gestation length for the odontocete sample revealed that there is no relationship between EQ and ges- tation length (Pearson r = -0.08). This finding is at variance with the pre- dictions from the r-K selection hypothesis that gestation length and EQ will be positively correlated. Also, the fact that there is no correlation between EQ and gestation length in the odontocete sample is not consistent with the positive correlation between EQ and gestation length found in primates (Ei- senberg 1981, Marino 1995).

An analysis of the correlation between body weight and gestation length in the odontocete sample revealed a significant positive correlation between body weight and gestation length (Pearson Y = 0.63, P < 0.01). This finding is

136 MARINE MAMMALSCIENCE,VOL. 13,N0. 1, 1997

consistent with an r-K selection pattern and is similar to that found in other mammals and, in particular, primates (Eisenberg 1981, Marino 1995).

Therefore, unlike that which is found in other mammals, especially pri- mates, EQ does not appear to be related to gestation length in odontocetes. In order to understand the discrepancy between the odontocetes and primates in terms of the relationship between EQ and gestation length, the relationship between EQ and body weight in the two groups must be compared. In pri- mates, there is no relationship between EQ and body weight (Marino 1995). In comparison, the present data show there is a moderately strong negative relationship between EQ and body weight among odontocetes (Pearson Y = -0.5 1, P < 0.058). That is, the smaller odontocete species tend to be more highly encephalized than the larger species. It is important to bear in mind that, unlike an uncorrected measure such as brain weight-body weight ratio, this effect exists even though the EQ measure already takes into account al- lometric relationships between brain size and body size, thereby apparently permitting direct comparisons across species.

Therefore, the relationship between EQ and body weight in odontocetes appears likely to involve factors over and above those found in primates. Al- though odontocetes are commensurate with primates in terms of their range of encephalization levels, body weight may be related to EQ in ways not found in primates and other mammals. One of the reasons for this may be the fact that body size increases in cetaceans are not subject to the same gravitational restrictions as those on terrestrial mammals. This has been suggested previ- ously by Economos (1983), Thompson (1942), and Worthy and Hickie ( 1986).

Taken together, these results suggest that the overall pattern of relationships between 11Q and the factors of gestation, body mass, and encephalization found in most mammals may not be predictive of the relationship among these factors within the odontocetes and most likely any of the Cetacea. It may be that a correction factor which takes into account non-allometric increases in body mass in cetaceans will need to be defined in order to interpret the relation between EQ and other life history factors in cetaceans in a manner comparable to terrestrial mammals. Also, additional relationships between EQ and other life history factors should be examined in cetaceans in order to determine the degree of similarity and dissimilarity between cetaceans and other mammals. A fuller understanding of life history patterns in cetaceans is importam both from a basic knowledge point of view and for the purposes of conservation.

ACKNOWLEDGMENTS

I wish to thank Charlie Potter and Jim Mead of the Marine Mammal Program, National Museum of Natural History, The Smithsonian Institution.

LITERATURE CITED

BEST, R. C., AND V. M. DA SILVA. 1989. Amazon river dolphin, Boto lnia geqfiensis (de Blainville, 1817). Pages 1-24 in S. H. Ridgway and R. Harrison, eds. Hand-

NOTES 137

book of marine mammals. Volume 4: River dolphins and the larger toothed whales. Academic Press, New York, NY.

BRYDEN, M. M. 1988. Adaptation to the aquatic environment. Pages 110-121 in R. Harrison and M. M. Bryden, eds. Whales, dolphins, and porpoises. Facts on File Publications, New York, NY.

CHEN IYU. 1979. On the cerebral anatomy of Chinese river dolphin, Lipotes vexillifer. Acta Hydrobiologica Sinica. 6:366-372.

CLU~ON-BROCK, T. H., AND P. H. HARVEY. 1980. Primates, brains, and ecology. Journal of Zoology (London) 190: 309-323.

DUNBAR, R. I. 1993. Coevolution of neocortical size, group size and language in humans. Behavioral and Brain Sciences 16: 681-735.

ECONOMOS, A. C. 1980. Taxonomic differences in the mammalian life span-body weight relationship and the problem of brain weight. Gerontology 26:90-98.

ECONOMOS, A. C. 1983. Elastic and/or geometric similarity in mammalian design. Journal of Theoretical Biology 103:167-172.

EISENBERG, J. F. 1981. The mammalian radiations. University of Chicago Press, Chi- cago, IL.

EISENBERG, J. F., AND D. E. WILSON. 1978. Relative brain size and feeding strategies in the Chiroptera. Evolution 32:740-75 1.

EISENBERG, J. F., AND D. E. WILSON. 1981. Relative brain size and demographic strategies in didelphid marsupials. The American Naturalist 118:1-15.

GASKIN, D. E. 1982. The ecology of whales and dolphins. Heinemann, London, U.K. GIBSON, K. R. 1986. Cognition, brain size, and the extraction of embedded food

resources. Pages 93-104 in J. G. Else and P. C. Lee, eds. Primate ontogeny, cognition, and social behavior. Cambridge University Press, Cambridge, U.K.

HAY, K. A., AND A. W. MANSFIELD. 1989. Narwhal Monodon monocero Linnaeus, 1758. Pages 145-176 in S. H. Ridgway and R. Harrison, eds. Handbook of marine mammals. Volume 4: River dolphins and the larger toothed whales. Academic Press, London, U.K.

HODOS, W. 1970. Evolutionary interpretation of neural and behavioral studies of living vertebrates. Pages 26-38 is Schmidt Neurosciences 2. Rockefeller Univer- sity Press, New York, NY.

JERISON, H. J. 1973. Evolution of the brain and intelligence. Academic Press, New York, NY.

KAMIYA, T., AND F. YAMASAKI. 1974. Organ weights of Pontoporia blainvillei and Pla- tanista gangetica (Platanistidae). Scientific Reports of the Whale Research Institute, Tokyo 32:105-126.

KRUGER, L. 1959. The thalamus of the dolphin Tursiops truncatus and comparison with other mammals. Journal of Comparative Neurology 3: 133-194.

LEATHERWOOD, S., AND R. R. REEVES. 1983. The Sierra Club handbook of whales and dolphins. Sierra Club Books, San Francisco, CA.

MACARTHUR, R. H., AND E. 0. WILSON. 1967. The theory of island biogeography. Princeton University Press, Princeton, NJ.

MACE, G. M., P. H., HARVEY AND T. H. CLUTTON-BROCK. 1980. Is brain size an ecological variable? Trends in Neuroscience:l93-196.

MANN, M. D., S. E. GLICKMAN AND A. L. TOWE. 1988. Brain/body relations among myomorph rodents. Brain and Behavioral Evolution 31:111-124.

MARINO, L. 1995. Brain-behavior relationships in cetaceans and primates: Implications for the evolution of complex intelligence. Ph.D. thesis, State University of New York, University at Albany, Albany, NY 488 pp.

MASTERTON, B., AND L. SKEEN. 1972. Origins of anthropoid intelligence: Prefrontal system and delayed alternation in hedgehog, tree shrew, and bush baby. Journal of Comparative Psychology 81:423-433.

MORGANE, P. J., AND M. S. JACOBS. 1972. Comparative anatomy of the cetacean ner-

138 MARINE MAMMAL SCIENCE, VOL. 13, NO. 1, 1997

vous system. Pages 118-244 in R. J. Harrison, ed. Functional anatomy of marine mammals: Volume 1. Academic Press, London, U.K.

PAGEL, M., AND P. HARVEY. 1989. Taxonomic differences in the scaling of brain on body weight among mammals. Science 244: 1589-1593.

PILLERI, G., AND R. BLJSNEL. 1969. Brain/body weight ratios in Delphinidae. Acta Anatomica 51:241-258.

PILLERI, G., AND M. GIHR. 1968. On the brain of the Amazon dolphin lnia geoffrensis de Blainville, 1817 (Cetacea, Susuidae). Experientia 24:932-934.

PILLERI, G., AND M. GIHR. 197Oa. The central nervous system of the Mysticete and Odontocete whales. Investigations on Cetacea 2:87-135.

PILLERI, G., AND M. GIHR. 19706. Brain-body weight ratio of Platanista gmgetica. Investigations on Cetacea 2179-82.

READ, A. J., R. S. WELLS, A. A. HOHN AND M. D. SCOTT. 1993. Patterns of growth in wild bottlenose dolphins, Tursiops truncatus. Journal of the Zoological Society of London 231:107-123.

RIDDELL, W. I., AND K. G. CORL. 1977. Comparative investigation of the relationship between cerebral indices and learning abilities. Brain, Behavior, and Evolution 14386~398.

RIDDELL, W. I., K. G. CORL AND F. GRAVETTER. 1976a. Cross-order comparisons using indices of cerebral development. Bulletin of the Psychonomic Society 8:22-24.

RIDDELL, W. I., F. GRAVETTER AND W. ROGERS. 19766. Further investigation of the relationship between brain indices and learning. Physiology and Behavior, 17: 231-234.

RIDGWAY, S. H. 1972. Mammals of the sea: Biology and medicine. Thomas, Spring- field, MA.

RIDGWAY, S. H. 1986. The central nervous system of the bottlenose dolphin. Pages 31-60 in R. J. Shusterman, J. A. Thomas and F. G. Wood, eds. Dolphin cognition and behavior: A comparative approach. Lawrence Erlbaum Associates, Hills- dale, NJ.

RIDGWAY, S. H., AND R. H. BROWNSON. 1979. Brain size and symmetry in three dolphin genera. Anatomical Record 193:664.

RIDGWAY, S. H., AND R. H. BROWNSON. 1984. Relative brain sizes and cortical surface areas in odontocetes. Acta Zoologica Fennica 172:149-152.

RIDGWAY, S. H., AND R. HARRISON. 1989. Handbook of marine mammals. Volume 4. River dolphins and the larger toothed whales. Academic Press, New York, NY.

RIDGWAY, S. H., N. FLANIGAN AND J. MCCORMICK. 1966. Brain-spinal cord ratios in porpoises: Possible correlations with intelligence and ecology. Psychonomic Sci- ence 6:491-492.

RIDGWAY, S. H., L. S. DEMSKI, T. H. BULLOCK AND M. SCHWANZEL-FUKUDA. 1987. The terminal nerve in odontocete cetaceans. Annals of the New York Academy of Sciences 519:201-212.

SACHER, A., AND E. F. STAFFELDT. 1974. Relation of gestation to brain weight for placental mammals: Implications for the theory of growth. The American Nat- uralist 108:593-615.

SAWAGUCHI, T., AND H. KUDO. 1990. Neocortical development and social structure in primates. Primates 31:283-289.

SLIJPER, E. T. 1979. Whales. Cornell University Press, Ithaca, NY THOMPSON, D. A. 1942. On growth and form. Cambridge University Press, Cam-

bridge, U.K. WORTHY, G. A., AND J. P. HICKIE. 1986. Relative brain size in marine mammals.

The American Naturalist 128:445--459.

LORI MARINO, Department of Biology, Emory University, Atlanta, Georgia 30322, U.S.A. Received 6 February 1996. Accepted 29 May 1996.