Brain and Life Span in Primates - allmanlab.caltech.edu€¦ · Five . Brain and Life Span in Primates . Atiya Hakeem, Gisela Rodriguez Sandoval, Marvin Jones, and John Allman . 1

Five

Brain and Life Span in Primates

Atiya Hakeem Gisela Rodriguez Sandoval Marvin Jones and John Allman

1 Introduction

Why is the brain so large in some primate species Brain size is well correlated with body size in primates but some primates such as humans and cebus monkeys have much larger brains than would be exshypected for their body sizes I t has long been postulated that species with larger brains tend to live longer (Friedenthal 1910 Sashycher 1959) We have found strong quanshytitative support for this proposition in higher primates [Allman in pressi Allshy

l- man McLaughlin amp Hakeem 1993ax 1993b see Section V in this chapter) Ourwf2w

tO~8 hypothesis is that the brain is a buffer gtQo against environmental variation Animals i8d that have longer life spans are likely to eftshyfgt-iltcar- perience more extreme environmental if shy fluctuations and thus be exposed during ~~~ ltcot the course of their longer lives to more seshyI~t vere crises (such as shortages in nonnallygO~gj used food resources) than animals with

shorter life spans Parts of the brain enable ill animals to store information about the enshy

~ vironment and develop cognitive strateshygies that enable them to switch to alternashytive food resources In this chapter we examine the ecological specializations linked to large brains and long life The

relative sizes of some brain structures such as the cerebellum and neocortex are particularly closely correlated with life span The cerebellum and some of these other highly correlated structures appear to be especially vulnerable to age-related dysfunction [see Allman in pressAllman et aL 1993b)

II Longevity in the Wild

Our analysis is based on the life spans of captive primates We have very little inforshymation on the longevity of primates in the wild because this requires sustained obshyservations of wild populations for many decades One of our concerns in using life spans of captive animals was that they might vary greatly from the species matishymum life span in the wild one might think that primates living in zoos would have longer maximum life spans than those living in the wild The few very longshyterm studies of primates living under natshyural conditions indicate however that some individuals do live into extreme old age in the wild Long-term observational data suggest that the maximum life spans for zoo-living and wild primates may be

Handbook of the Psychology of Aging Fourth Edition Copyright C 1996 Academic Press Inc All rights of reproduction in any form reserved

kPlEASE NOTE TiGHT BINDING 78

FIVE I Brain and Life Span in Primates

about the same Kenneth Glander (personshyal communication February 1 1993) has measured tooth wear in a wild population of 580 howler monkeys Alouatta palliata) in Costa Rica since 1970 Twelve of these monkeys have been under observation since 1970 In these old monkeys the teeth are all worn down to the gum line He estimates them to be between 24 and 28 years old The maximum life spans reshycorded for captive Alouatta species range from 20-25 years and thus appear tole fairly close to their longevity in the wild

Goodall (1986) observed 11 chimpanshyzees that she considered old at Gombe from 1965 through 1983 One of these was Flo who was a very successful individual with high-ranking offspring Figan and Fifi Flos teeth were worn down to the gum line and Goodall estimated her age four years before her death as II certainly more than 40 (p 104 see also Zihlman Morbeck amp Goodall 1990) Flos status and aggressive personality were strong facshytors in Figan and Pifis achievement of high rank Flo remained reproductive into old age but her last two offspring Flint and Flame did not flourish The infant Flame died during her motherS illness Flint although more than 8 years old at the time of his motherS death was unable to survive without her support For 8 years at Ranoinafana in Madagascar Patricia Wright (personal communication March 1 1993) observed a dominant female Proshypithecus diadema th~t she estimated on the basis of extreme tooth wear to be close to 30 years of age at the time of her death

Thus the limited data available from prishymates living in natural conditions indicate hat some individuals live into robust old

age Goodalls observations of Flo and her family also suggest that a parents longevishyty contributes to the success of the offshyspring even as adults and is likely to be a factor in the evolution of life spanshySustaining mechanisms in higher prishymates The parents longevity may be particularly important in catarrhine prishy

79

mates and especially in apes and humans because development is slow the period of dependence on the parents is long and even in adulthood the success of the offshyspring may be closely linked to parental status Because of late reproductive age long interbirth intervals and long periods of dependence on the mother female apes must live more than half the maximum reported life span for these species to maintain the population at the stable reshyplacement level (Goodall 1986 Ross 1991 Smuts Cheney Seyfarth Wranshygham amp Struhsaker 1987 see Table I) These factors may be responsible in part for the strong correlations between brain (and most brain structures) and life span in the group made up of gorillas orangutans chimpanzees and humans (see Table II) The selective pressure for maternal lonshygevity may also explain the predominance of females in our sample of very old prishy

~mates (Table I) and the much lower female mortality rates in contemporary human populations

III Brains Life Span and Diet

We have confirmed earlier studies that fruit-eating primates have significantly larger brains than leaf-eating primates (Clutton-Brock amp Harvey 1980) Fruitshyeating bats also have larger brains for their body size than insect eaters (Eisenberg amp Wilson 1978 PirIot amp Stephan 1970 Steshyphan Nelson amp Frahm 1981) A fruit eatshyers food supply is not constant because different plants bear fruit at different times and at different locations in the complex matrix of the tropical forest (MacKinnon 1975) An animal guided by memory of the locations of fruit-bearing trees can more efficiently exploit the available fruit resources than would othershywise be possible thus natural selection may have favored the development of cashypacities for visuospatial memory in frushygivorous primates (Allman 1977) This

--~ --- --------------------

Last Acquisition Acquisition Death response

Genus and species Agea age b date date SexC Animals name Facility or source date

Alouatta caraya 2025 L 25 41972 F Lincoln Park Zoo Chicago 8889 Illinois

Alouatta caraya 2000 L 3 82975 F April Twycross Zoo Atherstone 71992 Warwickshire England

Alouatta palliata 2500 L B Observations of Ken 1211193 Glander Costa Rica Wild

lUlation Alouatta pal1iata 2000 U Ross 11991) 2591 Alouatta senicuius 2500 U Ross (l991J 2591 Aotus trivirgatus 2525 L 7C 1676 312894 F Blanche Fleur Allman Lab Caltech Pasa- 312894

dena California Born at Crandon Park Zoo

Miami Florida co 0 Aotus tlivirgatlls 2000 U Ross 11991) 21591

Aotus trivirgaws 1925 L 2 1211176 F Zephyr Allman Lab Caltech Pasa- 1694 dena California

Arctocebus calabarensis 1217 91655 M The Zoological Society of London England

Arctocebus calabarensis 950 U Harvey Martin and Clutton-Brock 11987)

AleJes belzebuth 2800 L 2 11166 F Frances Twycross Zoo Atherstone 71992 Warwickshire England

Aleles belzebulh 2600 L 2 11167 F Ana tattoo 33 The Oakland Zoo in Know- 811191 land Park Oakland Calishyfornia

Aleles belzebulh 2600 L 2 11167 F Sigi tattoo 71 The Oakland Zoo in Know- 811 191 land Park Oakland Calishyfornia

AleJes tusciceps 2400 U Ross tI991) 21591 Aleles tusciceps 2150 L 49 101174 F Buddy 1068 Potter P~lrk Zoological Gar- 82091

dens Lansing Michigan Aides uscicejls 21()(J L YC HI2~79 M Junior 250 SellllOil PMk Zoo Eureka 811491

California

Table I Primate Life Spans

Born 84170 at National Zoo Washington DC

A I des geoff royi 4800 4C 4849 1119193 F Minnie Taronga Zoo Sydney 711092 Australia

Born in 1945 at Salt Lake City Zoo Utah

Atdes geolfroyi 3800 L 3 211457 F Munster Zoo Germany Ateles paniscus 3775 L 275 3657 F Artis Zoo Amsterdam The

Netherlands Atdes paniscus 3400 L 3 7659 F Vicky ISIS 21 Paignton Zoological amp Boshy 81191

tankal Gardens Paignshyton England

Cacajao calvus 2233 112858 33180 F Bronx Zoo New York Cacaiao calvus 1992 L 611672 U San Diego Zoo California 5119192 Cacaao melanocephalus 1800 L 11174 U KOln Zoo Germany Cacaao rubicWldus 2700 L 17 C 32381 M Los Angeles Zoo California 8191

Born 8365 at Milwaukee County Zoo Wisconsin

Cacl1iao wbiclmius 2lOO L 13 C 32381 F Los Angeles Zoo California 8191 IXgt Born 71069 at Milwaukee

County Zoo Wisconsin Callicebus moloch 2525 L 122165 M University of California at 2591

Davis California Calliceblls moloch 2025 L C 311572 F University of Kassel

Germany Born 311572 at Delta Prishy

mate Center Covington Louisiana

Callimico goddii 1790 U Ross (1991) 215191 Callimico goeIdii 16lO 411369 512885 F Frankfurt Zoologischer Garshy 727192

ten Germany Callimico goeldii 1575 L 75 711U77 M Pepe Brookfield Zoo Chicago 712192

Zoological Society Illishynois

Callitbrix argentata 1683 17 711868 912383 F Birmingham Zoo Alabama Callitluix argentata 875 612251 331160 U Bronx Zoo New York Callitbrix bumeralifer 1500 11165 71180 U Adelaide Zoo Australia

(continuesl

r

Thble I

Last Acquisition Acqu isi tion Death response

Genus and species Age agel date date Sex Animals name Facility or source date

Callitllrix jacchus 1675 58 711166 911182 M Frank Rossi (private party) Gravesend Kent England

Callithrix acchlls 1566 C 211168 U Birmingham Zoo Alabama

Cebuella pygmaea 1810 51768 61486 M Japanese Primate Center 111190 Aichi Japan

Cebuella pygmaea 1508 L 812477 F Stichting-Apenheul 912192 Apeldoorn Holland

Cebus albifrons 4400 U Ross 11991) 25191

Cebus albifrons 4050 5 611049 612089 F Squeaky Sue Norton (private party) 612089 South Pasadena Calishyfornia

Cebus albifrolls 2500 L C 811066 M OmahaS Henry Doorly 7119191 Zoo Omaha Nebraska

00 Cebus apella 4510 511234 6116179 M Mil waukee County Zoo tI

Wisconsin Cebus apella 4100 4 111127 512464 M Irish San Diego Zoo California Cebus capucillllS 5475 1 111135 ]04188 M Hobu Lederle Labs Pearl River

New York Cebus capucinus 4692 511129 41676 M Evansville Zoo Indiana Cebus nigrivittatus 4100 L 71152 F Santa Ana Zoo California 61589

Cercocebus albigena 3270 U Ross (1991) 215191 Cercocebus albigena 3266 111930 912362 M San Diego Zoo California Cercocebus albigena 2100 U Harvey Martin and

Clutton-Brock Cercocebus aterrimus 2675 41954 213181 M Cercocebus atys 2675 M Cercocebus atys 1800 U

Clutton-Brock (1987) Cercocebus galeritus 2100 L 5 4112175 F June Sacramento Zoo California 711191

Cercocebus Jlaleritus 1900 U Harvey Martin and 11187 Clutton-Brock (1987)

Cercocebus galeril liS 1900 U Ross (19911 215191

Ccmocebus IOlltllll us 2700 U Ross 19911 215191

(tImiddotoceJlls t)r~J ~((llS

Cercoceims torquat us

Cercopithecus aethiops



Cercopithecus ascanius Cercopithecus ascallius Cercopithecus cam belli

Cercopithecus cephus

00 (JJ


Cercopithecus diana

CercopitilCclls diltlllltl

Cercopithecus diana

Cercopithecus hamiyni

Cercopithecus mitis

Cercopithecus mitis

Cercopitheclls muna

2050

1470 L

3160 L

3100

2300 L

2825 2592 2500 L

2300 L

2300 L

3725

480

3000 L

2700

2710 L

2500 L

2200

47

13 C

4

25 2233

2

33)

333

5

21

417

71611

411174

21872

811458 43084 519155

1212272

1212272

11140

2466

912980

6121166

1112171

U

f

M Aba

U

M Jonathan

1212485 12887

F F F

F

Nosy

M

U

U

F Dora

711185 M

F

F

Sarah 192

U

f

lInrvcy Martin ami 1 Ill 7 Cll1tton-Brock 19H7)

-Micke Grove Zoo Locli 7123191 -California

Jerusalem Biblical Zoo 712891 Ltd Romema Jerusalem Israel

Born 11160 at Haddassah Harvey Martin and

Clutton-Brock (i987J The Oakland Zoo in Know- 7191

land Park Oakland Calishyfornia

Birmingham Zoo Alabama San Diego Zoo California Jardin Zoologique de Que- 829191

bec Canada Louisiana Purchase Gardens 819192

and Zoo Monroe Louishysiana

Louisiana Purchase Gardens 8119192 and Zoo Monroe Louishysiana

Miami Monkey Jungle Flor- 1111177 ida

Harvey Martin and Clutton-Brock (19871

Audubon Zoological Gar- 7119191 dens New Orleans Louishysiana

San Diego Zoo San Diego California

Omahas Henry Doorly 712892 Zoo Omaha Nebraska

Lousiana Purchase Gardens 81992 and Zoo Munroe Louishysiana

Ross (1991) 2591

kontinues)

Table I


Genus and species Age a agelgt date date Sexc Animals name Facility or source date

Cercopithecus mona 2050 L 18 C 312488 F Lisa Dallas Zoo Texas 6192 Born 1219170 at Bronx

Zoo New York Cercopithecus neglect1s 2625 L 47 5125170 F Sacramento Zoo California 211292

Cercopithecus neglectus 2300 L 15 717170 F Countess Denver Zoological Gardens 712992 Colorado

Cercopithecus nictitans 2300 L 3 1119171 F Greater Baton Rouge Zoo 711991 Baker Louisiana

Cercopithecus nictitans 1892 L 2 9572 M Speedy Gonzalez Jardin Zoologique de Queshy 812991 bee Canada

Cercopithecus petaurisla 1900 U Houston Zoological Garshydens Texas

00 Cercopithecus petaurista Cercopithecus pogonias

1617 L 2410 L

4 17

228179 6684

F F

Serena LRZ936 The Zoo of Arkansas Cincinnati Zoo amp Botanical

61191 611191

Gardens Ohio Cercopitheclls pogonias 1850 C 512870 1124R9 F Cincinnati Zoo amp Botanical 611191

Gardens Ohio Cercopithecus talapoin 3087 22 10639 611967 M Philadelphia Zoological 730192

Garden Pennsylvania Cercopithecus Lalapoin 2308 L 155 C 911383 M Beck 83MI36 Buffalo Zoological Gardens 7120191

New York Born 3968 at Brookfield

Zoo Illinois

Cheirogaleus major 1500 U Martin 11984) Cheirogaleus major 1000 L 3 1184 F Rapunzel Duke University Primate

Center Durham North 811191

Carolina Cheirogaleus major 866 51352 112261 U The Zoological Society of

London England Cheirogalells medius 1925 L C 411373 M Jesse 606 Duke University Primate


Cuolina Cljir()~(IelN lIIedill8 17()O L C 71HI7t1 F Dim 611pound Duke University lrimate 811191

~ Io~- Center Durham North Carolina

Chiropotes albinasus 1166 F Kaln Zoo Germany 111177 Ciliropotes satanas 1500 F San Diego Zoo California Chiropotes satanas 1266 M Kaln Zoo Germany 111177 Colobus guereza 2450 1 101140 417164 M San Diego Zoo California Colobus guereza 2375 C 411450 25174 F San Diego Zoo California Colobus polykomos 3050 U Ross (1991) 21591 Colobus polykomos 2600 U Harvey Martin and

Clutton-Brock (19871 Colobus polykomos 2400 L 23 4490 M Sikasso A1123 The Zoological Society of 630191

London England Cynopithecus niger 2850 L 54 51069 F Faith 613 Omahas Henry Doorly 72892

Zoo Nebraska Cynopithecus niger 1800 U Harvey Martin and

Clutton-Brock Daubentollia madagasshy 2425 6314 911537 U Artis Zoo Amsterdam The

cariensis Netherlands Daubelltollia madagasshy 540 L 24 11188 F Samantha Duke University Primate 815191

(Xl

VI cariensis Center Durham North Carolina

Erythrocebus patas 2392 33164 225188 F Jardin Zoologique de Queshy 829191 bee Canada

Erythrocebus patas 2166 82270 411892 F Artis Zoo Amsterdam The Netherlands

Erythrocebus patas 2166 115155 811276 F Frankfurt Zoologischer Garshy 72792 ten Germany

Galago crassicaudatus 1875 C 102468 7117187 M Barney Houston Zoo Gardens 911587 pers petmiddot of J Banks Texas

Galago crassicaudatus 1800 C 22466 3884 M Artis Zoo Amsterdam The Netherlands

Galago demidovii 1400 U Harvey Martin and Clutton-Brock

Galago demidovii 942 U Private Galago demidovii 916 F Brookfield Zoo Chicago


(continues)

1

DIble I Continued)


Genus and species Age agel date date SexC Animals name Facility or source date

Galago senegalensis 1700 L 13 C 61086 F Cincinnati Zoo amp Botanical 5192 Gardens Ohio

Born 7173 at Buffalo Zoo New York

Galago senegalensis 1650 12 62173 San Antonio Zoological Garden amp Aquarium Texas

Gorilla gorilla gorilla 5400 5 123035 1231184 M Massa Philadelphia Zoological 73092 Glrdeu Pcnnsylvania

Gorilla gorilla gQrilla 4700 43 1182 912786 F Carolyn Bronx Zoo New York 121086

Hapalemur griseus 17lOL C 6123175 F Befuddled DlIke University Primate 6192 Center Durham North Carolina

00 Hapalemur griseus 1275 82064 M Koln Zoo Germany 0 Homo sapiens 12060 0 6291865 2121186 M S Isumi The Guiness Book of Reshy 11192

Homo sapiens 10500 U Max 1000 Angeles Times

Hylobates agilis 4400 L 121249 M Nippy MlO Wellington Zoological Garshy 71592 dens New Zealand

Hylobates agilis 2800 L 6 lOill7o F Twycross Zoo Atherstone 7992 Warwickshire England

Hylobates concoior 4410 9337 10121181 U Vincennes-Pare Zoologique de Paris France

Hylobates concolor 2500 L 23 101289 F Mizzi Safari park Beekse Bergen 1130192 Hilvarenbeek The Netherlends

Hylobates lar 4000 L 2 Ill54 M Samson San Antonio Zoological 711392 Garden amp Aquarium Texas

llyiowles Jilr 4000 L 2 IIt S4 F Samantha San Anwnio Zoological 7L)2 Clrdcn amp Alillarilllll TCX1S ~

lIyubales llWcXJI

muelleri Hylobates molocb

muelleri

Hylobates moloch muelleri

Hylobales pileatus

Hylobales pileaws Hylobates pileatus

x agilis Hylobates syndactylus

Hylobates syndacty1us

Lagotbrix lagoricilll

00 Lagothrix lagotricJw -j

Lagotllrix lagotricha

Lemur calta

Lemur catta

Lemur catta

Lemur COfOnatus Lemur fulvus

Lemur fulvus

Lemur macaco Lemur macaco

290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U

Twycross Zoo Atherstone 7992 Wnrwiekshire England

San Antonio Zoological 8591 Gardcn amp Aquarium Texas

San Antonio Zoological 8591 Garden amp Aquarium Texas

1vycross Zoo Atherstone 7992 Warwickshire England

Phocnix Zoo Arizona 72391 National Zoo Washington

DC Milwaukee County Zoo 92292

Wisconsin Milwaukee County Zoo 92292

Wisconsin Thc Monkcy Sanctuary

Looe Cornwall England Ross (1991) 2591 Royal Zoological Socicty of

Antwerp Belgium Buffalo Zoological Gardens 71l492

New York Harvcy Martin and

Clutton-Brock 11987) Mesa College San Diego

California Born 1264 at San Diego

Zoo California Giza Zoo Egypt Buffalo Zoological Gardens 8988

New York Duke University Primate 6192

Center Durham North Carolina

St Louis Zoo Missouri Harvey Martin and

Clutton-Brock (19a7)

(continues)

-- -----~~------- _w4~o~--~~~--~_____

Table I ( Continued)

Last Acquisition Acquisition Death responseGenus and species Age agel date date SexC Animals name Facility or source date

Lemur maeaeo 2708 111110 11137 F Buffalo Zoological Gardens

Lemur maeaeo x fulvus 3900 U New York

Buffalo Zoological Gardens

Lem tlr mongoz 2790 L 8112164 M New York

Philadelphia Zoological 712391

Lemur mongoz Lemur variegatus

2425 3200 L 2 61262

U F Saturna 524f

Garden Pennsylvania St Louis Zoo Missouri Duke University Primate 6192

Center Durham North

Lemur variegatus 2800 M Carolina

The Zoological Society of 512389 London England

OQ 00 Born 512669 at San Diego

Leontopitheeus rosalia 2475 L 46 C 411172 M Houston Zoo California


Born 10117167 at Houston

Leontopithecus rosalia Loris tardigradtls

2200 1640

622164 619174

8111186 1112489

F M

Zoological Gardens Texas Los Angeles Zoo California The Zoological Society of

121086 85192

Loris tardigradus 1400 L 72678 M London England

Frankfurt Zoologischer Garo 719192

Afacaea arctoides Afacaea aretoides

3000 3000

U U

ten Germany Ross (1991) Harvey Martin and

25191

Macaea arctoides 2400 L 511168 F Pat 88063 Clutton-Brock (1987)

Catoctin Moutain Zoologio 6192 cal Park Thurmont

Macaca aretoides MacaclsciclIaris Mliclc( Ilscicllillris

2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland

Racine Zoo Wisconsin Ross (lYY I) Prl1 (nn 1111

BillY I 25191

Mac4ca lasccultlris 2500 ~9 MI69 121 I 90 F Charlcs Paddock Zou Atasmiddot 619 cadcm California

Macllca tuscaLa ~300 8113 U Kagoshinla Japan IPrimate Iifespans 1966)

Macaca tuscata 3300 U Ross 11991) 2591 Macaca tUSCOLa 2266 L 6 630175 F Grandma Fo]somChildrens Zoo Lin- 61191

coin Nebraska Macaca mulatta 3600 U Ershler et aJ (1988) Macaca mulatta 3500 U Tigges Gordon McClure

Hall and Peters 11988) Macaca mulatta 2600 L C 10965 U Micke Grove Zoo Lodi 72391

California Macaca mulatta 2300 L 25 10965 F Micke Grove Zoo Lodi 723191

California Macaca nemestrina 3433 L 511156 U Japanese Primate Center 1190

Aichi Japan Macaca nemestrina 2707 39 6167 51292 M Joco Reid Park Zoo TUcson Ari- 51l292

zona Macaca silenus 4000 37 12586 4389 F Baltimore Zoo Maryland 61191

00 Macaca silenus 3800 37 121586 51187 M Baltimore Zoo Maryland 611191 0 Macaco sinica 3000 Ross (1991)

Macaca sinica 2933 U Colombo Sri Lanka Macaca sylvania 2200 Ross (1991) Macaca sylvania 1700 L C 7115174 M Kenneth Paignton Zoological amp Bo- 811191

tanical Gardens Paignshyton England

Microcebus murinus 1550 25 C 12121177 910191 M The Zoological Society of 719192 Londoll England

Born in 1975 at Wellcom Laboratory London Enshygland

Microcebus murinus 1550 U Harvey Martin and Clutton-Brock (1987)

Microcebus murinus 1400 L C 813177 M Snout 837m Duke University Primate 8591 Center Durham North Carolina

Mirza (MiclOcebus) co- 1525 U The Zoological Society of London

(continues)

ltr

Iable I


Genus ami species Age Q age b date date Sex Animals name Facility or source date

Nasalis lalvaLUs 210 3 712667 811585 M Jimmy 001116 Dallas Zoo Texas 1111692 Nasalis lalvatus 2000 L 18 21690 F Barabara Wilhelma Zoological Gar- 712492

den Stuttgart Germany Nycticebus coucang 2650 412363 F Artis Zoo Amsterdam The

Netherlands Nycticebus coucang 2000 7 4121177 6590 F REM 20680 Woodland Park Zoo Seattle 7992

Washington Owlemul (Calago) 1566 L 11120Z6 M University of Kassel Gershy

garnetli many Owernul (Caago) 1500 1058 51876 10280 F University of Kassel Gershy

garnetti many

Pan troglodytes 5940 C 92132 21992 F Gamma Yerkes Reg Primate Resrch Ctr Emory Univ Atlanshy

a 0 ta Georgia Pan troglodytes 5600 2 71131 911785 M Jimmy Rochester Zoo New York Papio anubis 2517 M S1Il Dilgo Zoo California Papfo cynocephalus 4000 U Ross (1991) 2591 Papio cynocephalus 3510 L 8444 F Japanese Primate Center Ill9O

Aichi Japan Papio cynocephalus 2766 U Bronx Zoo New York Papio hamadlyas 3750 611135 122772 M Brookfidd Zoo

Zoological Society Illishyno is

Papio hamadlyas 3560 U Harvey Martin and Clutton-Brock (1987)

Papio hamadlyas 2883 125 5833 11461 U Calgary Zoo Alberta Canada Papio leucophQeus 3342 25 111150 11180 F Rome Zoological Garden

Italy Papio leucophaeus 2860 U Harvey Martin and

Clutton-Brock (1987) Papio leucophaeus 2842 7333 1112261 U Milwaukee County Zoo

WbcIlilsin Iipill IltllJiu 1000 IJ Ioss jI )) I ) 215)1

Papio papiD 2700 11164 a1191 M Unclc+ Brookficld Zoo Chicago 8591 Zoological Society lllinois

Papia papia 2580 U National Zool Gardens of S A Pretoria South Africa

Papia sphinx 3166 62334 31866 F Kumamoto Japan (Primate life spans 1966)

Papia spllinx 3141 C 62444 1211175 F Philadelphia Zoological Garden Pennsylvania

Papia ursinus 3120 L 71159 F Japanese Primate Center 111190 Aichi Japan

Papia ursinus 2758 U Philadelphia Zoological Garden Pennsylvania

PerodicticlIs potto 2600 15 12 159 711684 M Pittsburgh Zoo Pennsylvania

PerodicUcus potto 2200 11 152 62674 M Basel Zoological Gardens Switzerland

Phaller fUlcifer 1200 U Observations by Dr J Petter Pithecia monachus 2460 4 71464 511085 F San Diego Zoo California

0 Pithecia pithecia 2066 L 1 112672 M Timmy Denver Zoological Gardens 729192 Colorado

jJilhecia pilhecia 1800 L 2 625175 M Ron A258 The Zoological Society of 73091 London England

Pithecia pilhecia 1800 L 2 6125175 F Barbara A259 The Zoological Society of 73091 London England

Pongo pygmaellS 5875 13 51131 2977 M Guas 100001 Philadelphia Zoological 73092 Garden Pennsylvania

Pongo pygmaeus 5725 13 5 [31 1116176 F Guarina 100002 Philadelphia Zoological 730192 Garden Pennsylvania

jJresbytis cristata 3108 C 21245 3176 F San Diego Zoo California 717194 Born 21245 at San Diego

Zoo California Presby tis cristata 1883 L 7C 911780 M Los Angeles Zoo California 81492

Born 10118173 at San Diego Zoo California

Presbytis entellls 2500 11142 F Miami Monkey Jungle Florida

(continues)

1

MItKciliu t kiM fMe f ted

Idble I Continued)


Genus and species Agea ageb date date Sexc Animals name Facility or source date

Presby tis entellus 2400 3 33164 42585 M San Diego Zoo California Presby tis melalophos 1600 U San Diego Zoo California Presby tis obscura 2500 L 1858 6686 U Artis Zoo Amsterdam The

Netherlands Presby tis obscqra 1533 L 7C 51183 F June Point Defiance Zoo amp 72091

Aquarium Tacoma Washington

Presby tis senex 2300 L 15 212885 M Greater Baton Rouge Zoo 71991 Baker Louisiana

Propithecus verreauxi 2060 L C 210172 M Nigel 597m Duke University Primate 6192

QN


Propithecus verreauxi 1817 F Duke University Primate Center Durham North Carolina

Pygathrix nemaeus 2500 L 6868 M Kaln Zoo Germany pygathrix nemaeus 2100 L 325170 M Peter Wilhelma Zoological Garshy 72491

den Stuttgart Germany Saguinus fuscicolJis 2450 117 8569 31392 F Jersey Wildlife Preservation 1493

Trust Jersey Channel lsshylands

Saguinus fuscicollis 2040 C 2112168 7388 F University of Tennessee 72792 Knoxville Tennessee

Saguinus imperator immiddot 2017 61061 9781 M Jersey Wildlife Preservation perator Trust Jersey Channel Isshy

lands Saguinus imperator immiddot 1300 101462 10114175 M Frankfurt Zoologischer Garshy

perator ten Germany SaguilUIS nigricolis 1520 411H61 715176 f Brookfield Zoo Chicago

Zooillgical Socilty illishynois

__ ~agllilluS Iligluiiis JLOIl 41H61 6110172 U nruokflcld Zoo Chicago Zoological Socicty Illishynois

Saguinus oedipus 208 L 6117170 M Jimmy Denver Zoological Gardens 712992 Colorado

Saguinus oedipus 2295 L 95 1231167 U St Paul Zoo Minnesota Saguinus tamarin 1540 11964 411480 M Zurich Zoologischer Gar-

ten Switzerland SagullJUs tamarin 13)7 F Zurich Zoologischer Gar-

ten Switzerland Salmiri sciureus 2700 1 lI67 1l2984 F Miss Baker Alabama Space and Rocket

Center Huntsville Alashybama

Salmiri sciureus 2266 25 lI560 31980 M WD-l Woodland Park Zoo Seattle 7992 Washington

Tarsius spectrum 1200 U Ross (1991) 21591 Tarsius spectrum 1200 U Harvey Martin and

Clutton-Brock (1987) Tarsius syrichta 1500 4 51683 12193 M Amos Duke University Primate

0 Center Durham North Vgt

Carolina Tarsius syrichta 1350 5864 101477 M Frankfurt Zoologischer Gar-

ten Germany Tlleropithecus gelada 2800 L 2 21565 F San Antonio Zoological 81591

Garden amp Aquarium Texas

Theropithecus gelada 2700 L C 102865 F Zurich Zoologischer Gar-ten Switzerland

aL the animal was still alive at the time of the last response bC Captive born cF female B both males and females M male U unknown sex

T

94 A Hakeem G Rodriguez Sandoval M Jones amp J Allman

Table II Correlations between Brain Structure Volume Residuals and Life Span Residuals for Gorillas

Orangutans Chimpanzees and Humans

Brain structure r p

Brain whole 0997 00008 Cerebellum whole 0985 00152 Diencephalon 0990 00077 Hippocampus 0946 00738 Medulla 0988 amos Mesencephalon 0991 00064 Neocortex 0989 00087 Striatum 0994 00041

study has shown that fruit eaters also live significantly longer lives than do leaf eatshyers when the effect of body size is reshymoved Because of the ubiquitous nature of leaves the computational and memory requirements necessary to support a leaf eater might be less than the requirements to support a fruit eater of the same body size

There is evidence for a budgetary tradeshyoff between energy devoted to mental acshytivity (brain metabolism) and energy deshyvoted to digestion This proposition may be obvious to anyone who has felt groggy while digesting a large meaL This trade-off arises from the fact that the energy conshysumption of the whole organism is closely related to body mass and therefore ex- pansion of one energy-expensive tissue must be compensated by a neduction in other expensive tissues (Aeillo amp Wheeshyler 1995) In haplorhine prImates body weight-digestive organ weight residuals are significantly negatively correlated with body-brain weight residuals (I =

-069 p lt 0001 n = 18 Aiello amp Wheeshyler 1995) Thus haplorhine primates with large guts for their body size tend to have small brains The size of the digestive orshygans is in tum related to the complexity of the foods to be digested Difficult-to-digest foods such as leaves require a large gut whereas easy-to-digest foods such as ripe fruit and meat require a smaller gut Thus

to have a large brain an animal would tend to have a small gut and a correspondingly rich easily digested diet The greater diffishyculty in obtaining sufficient quantities of energy-rich easily digested foods in tum would be a selective factor favoring the deshyvelopment of a larger brain

In the plot of relative gut mass to relashytive brain mass (Aiello amp Wheeler 1995) it is striking that the primate with the largshyest brain and smallest gut Homo sapiens is also the longest lived In this same figure from Aiello and Wheeler the species closshyest to Homo sapiens is Cebus apella Figshyure 1 plots relative life span to relative brain weight the cluster of three data points nearest to Homo sapiens are three species of Cebus which like humans also have small guts and an energy-rich diet At the opposite [lower left) end of the graph in Figure 1 the small-brained and short-lived species are all leaf eaters which tend to have large guts (Aiello amp Wheeler 1995 Chivers amp Hladik 1980) Thus there apshypears to be an energy budgetary trade-off such that an organism must devote more of its energy to the digestion of readily available hard-to-digest foods or altershynatively to the task of acquiring foods that are less available and easy to digest The search for foods that are both less available and also rich and easily digested requires a larger brain These observations led us to test the hypotheSiS that relative gut size would also be negatively correlated with relative life span Using Aiello and Wheeshylers gut data we calculated the gut-body residuals and compared them with our life span-body residuals We found they were not significantly correlated (I = -0169 p = 0477 n == 19) However the distribushytion of the data revealed that there were no haplorhine primates with relatively large guts and long life spans for their body weight

We found no relationship between basal metabolic rate [BMR) and maximum life span in primates when the effect of body weight was removed Austad and Fischer

FIVE Brain and Life Span in Primates

15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull

bullbullbull bullbull bull

q

bull

bullbull

bull

+ Homo sapiens Insect Eaters bull Fruit Eaters o Leaf Eaters o Siamang

95

05 06 07 08 09 10 11 12 13 14 15

Brain Weight Residuals Figure 1 Life span residuals versus brain weight residuals for haplorhine primates [Martin data setI IN =50 r = 0640p lt 0001 slope of major axis regression 1014) Species data points are labeled according to diet type

The siamang IHylobates syndactylus) has dietary proportions of 435 fruit and 4375 leaves (average of studies reported in Smuts et al 1987) It was omitted from the dietary statistical analyses because its extremely similar dietary proportions made it difficult to classify

(1991) showed that the exceptional lonshygevity of bats relative to a large sample of nonflying eutherian mammals is not reshylated to BMR These authors have also shown that although marsupials have sigshynificantly lower BMRs than eutherian mammals they have shorter life spans when the effect of body mass is taken into account These findings contradict the popular idea that animals with high BMRs burn out more quickly which in scientific arlance has been termed the rate of livshying hypothesis of longevity (see Finch 1990 for a review) It is still conceivable that the well-established relationship beshytween body mass and longevity is someshyhow related to the higher BMRs in smaller ~als which might for example result 1ll the more rapid generation of toxic byshyproducts and thus accelerate the aging proshy

cessj however our findings and those of Austad and Fischer (1991) provided no supshyport for the prediction of the rate of livshying hypothesis that animals with higher BMRs than would be expected for their body masses have shorter life spans We suspect moreover that the relationship between body mass and longevity is due to the greater vulnerability of smaller anishymals to predation starvation and intoxshyication by plant poisons (see Section IV)

IV Specializations Enhancing Longevity in Birds

and Mammals

The relationship between brain and life span is confined to the haplorhine primates (tarsiers monkeys apes and humans) and

96 A Hakeem G Rodriguez Sandoval M Jones amp J Alima

is especially strong in the group made up of the great apes and humans [Allman in preSSj Allman et al 1993a Section V of this chapter) The lack of correlation in strepsirhines (lorises and lemurs) may be due to the fact that all strepsirhine speshycies are nocturnal or native to the island of Madagascar (or both) Nocturnality and island habitat probably result in both less competition for food resources and less predation pressure by other animals and this may account for the lack of corshyrelation between brain and life span residshyuals in lower primates Alternatively the relationship between brain and life span may be a specialization in higher primttes It is important to analyze relationships beshytween brain and life span in other groups of mammals Austad and Fischer [1992) found that the relationship between brain and life span was much stronger for prishymates than other mammals In a prelimishynary survey of bats and insectivores we found no correlation between brain and life span residuals It is possible that the strong linkage between brain and life span is unique to higher primates or conceivshyably limited to a few groups of animals yet to be determined

Another biological specialization linked to longevity is flight Francis Bacon (1638) commented extensively on the great lonshygevity of birds Factoring out body weight the average maximum life span for avian species is more than twice as long as for eutherian mammals [Lindstedt amp Calder 1976) Similarly maximum longevity in bats averages three times that of nonflying eutherian mammals gliding mammals average 17 times the average maximum life span of nonflying eutherians and arboshyreal marsupials have significantly longer life spans than terrestrial marsupials (Ausshytad amp Fischer 1991) The capacity for flight gliding or arboreality potentially reduces the risks of predation and opens up new means for gaining access to food reshysources These capacities are analogous to expanded brain size in higher primates in

that they are energetically expensive ada tations that reduce vulnerability to th hazards of predation and starvation

A recent theory of life history hypothe sizes that the rate of senescence is detel mined by the extrinsic adult mortali ty rat [ie by deaths resulting from predatior environmental hazards and other factor not related to the reproductive efforts 0

the organism) (Charnov 1991 j Hill 1993 Promislow amp Harvey 1990) This theoryi substantiated by the finding that opos sums living on an island with reduced ex posure to predation live longer and have slower acceleration of age-specific mortal ity rates than do opossums living on thf mainland where they are exposed to the full range of predators (Austad 1993) There is also evidence that the biochemimiddot cal mechanisms of senescence are retarded in the island -dwelling opossums because the age-specific deterioration of collagen fimiddot bers is slower in them than in the mainland opossums [Austad 1993) This theoretical linkage between increased environmental hazards and accelerated senescence may also explain the shorter life spans in folishyvores because they ingest large quantities of plant toxins in their diet In conclUSion we suggest that the ability to fly and enshylarged brains are specializations that reshyduce the vulnerability in some groups of endothermic vertebrates to the hazards of predation and starvation and that the deshyvelopment of these capacities is linked to the retardation of the rate of senescence and to increased longevity

V Primate Brain and Life Span Database

We used the maximum recorded life span because it should measure under ideal cirshycumstances the genetic potential for lonshygevity for each species Agemiddotspecific morshytality or even average life span data are not available for a large enough sample of speshy


cies to conduct this analysis We collected a database of life spans for primate species by querying zoos and research institutions throughout the world Our queries were guided by records from the International Species Inventory System (ISIS) and by the records of one of the authors (MJ) The ISIS database does not keep track of ages greatshyer than 20 years which is less than the maximum life span for most primate speshycies We queried zoos for ages for the oldest ISIS-listed animals where the maximum listed life span was less than 20 years and for all animals listed in ISIS as over 20 as well as for old animals in personal records We next sent out requests for more details (such as dates and animal IDs) about the oldest animals of each species as identishyfied by our preliminary questionnaires We also used some life span da ta from Ross 119881991) and from Harvey Martin and Clutton-Brock (1987) when these data gave a longer life span for a species than we otherwise had The maximum docushy

mentedhuman life span is 1206 years (Matthews 1994) however this is based on a population about a million times largshyer than that for any nonhuman primate Therefore we used a value from a contemshyporary human population more nearly comparable in size to the populations of nonhuman primates sampled In a sample of 1000 obituary notices published from August 1991 through June 1993 in the Los Angeles Times the longest lived individushyal was 105 years old IObituary 1992)

The quality of the life span data is limshyited by three major factors First the samshyple sizes for rare species were relatively small We believe that the extremely high correlations between brain structure and life span residuals we found in the great apes and humans (see Table II) were in part due to the large sample sizes and high quality of record keeping for this group Second many of the long-lived animals in our survey were born in the wild and their age at acquisition could only be estimated We accepted the zoos estimate of the age

97

at which an animal was acquired for anishymals that were acquired while immature For animals acquired from the wild as adults we used a value for adult age as the age at acquisition Our value of the adult age was the average age of females at first reproduction for the species from a table by Ross (1988 1991) If the zoo had evishydence such as extreme tooth wear or havshying borne several offspring to indicate that the animal was older than the female age at first reproduction when it was acquired we adjusted the estimated age at acquisishytion accordingly

In particular since our earlier publicashytions we have adjusted our maximum life span for the orangutan upwards as we learned that the record-holding animal Guas was a mature male with cheek pads when he was acquired by the Philadelphia Zoo According to Dr Birute Galdikas (personal communication March 11994) 1

the minimum age for a male orangutan to develop cheek pads is 13 so we used 13 as Guass estimated age at acquisition It is possible that he and his mate Guarina were older when acquired but we prefer to use the most conservative estimate conshysistent with the available information This change in our maximum life span valshyue for the orangutan the use of maximum human life span from a sample size comshyparable to that available for nonhuman primates and changes in the maximum life span values for a few other species for which we have received additional records have slightly changed our resulting corshyrelation values from those we have pubshylished before [Allman 1995 i Allman et al 1993a 1993b) The third major factor limshyiting the quality of the life span data is that because of improved husbandry in 36 species the maximum life span record is for a living animal Thus the maximum life spans will necessarily be underestishymated for these species

Table I is a compendium of our data inshycluding the vital statistics for the first and second longest-lived individuals for 112


primate species In cases where the first or second record for a species was from a pubshylication rather than from a zoo record the top two zoo records are also listed if availshyable In the sample of very old primates in the cases for which gender was known there was a preponderance of females over males (F = 94 M = 73)

We tested the hypothesis that brain weight is correlated with life span when the effect of body weight is removed We used brain and body weight data from an unpublished database compiled by Prof R D Martin and his colleagues at the Unishyversity of Zurich We also used data from Stephan and his collaborators Baron Frahm Bhatnagar Kunwar amp Stephan 1983 Frahm Stephan amp Baron 1984 Frahm Stephan amp Stephan 1982 Matashyno Baron Stephan amp Frahm 1985 Steshyphan Baron amp Frahm 1982 Stephan Frahm ampBaron 1981 1984 1987) on body

40

30

l)I

fa 00 2 c middote =I

j 10

00 10 20 30

weights and the volumes of various brain structures to determine which structures are correlated with life span We obtained BMRs from an unpublished database comshypiled by Prof Martin We also used pineal volumes from Stephan Frahm and Baron ( 1981) surface areas of the posterior half of the eye (Stephan et al 1984) and testes weights (Harrison amp Lewis 1986) Because life span brain weight and these other measures are all correlated with body weight (Allman et aL 1993a 1993b) it was necessary to remove the effect of body weight to observe the net effect of variashytion in the size of the brain its composhynents and the other measures on life span Data on diet in primate species were obshytained from Smuts et al (1987)

Figure 2 illustrates the relationship beshytween body and brain weight Figure 3 ilshylustrates the relationship between body weight and life span To remove the effect


40 50 60

Log Body Weight g

Figure 2 Log brain weight in grams versus log body weight for the entire set of primate species for which we have data (N = 72 r = 0970 p = 0001 slope = 0803) The effects of body weight were removed by calcumiddot lating the residuals from the least-squares regression line

FIVE I Brain and Life Span in Primates 99

22

20 +

18 bulli

bullQgt

16C rI

C tfl ~ s 14 bullbull ~

+ Homo sapiens OIl

oS 0 Insect Eaters

bull bull bull Fruit Eaters 12

o Leaf Eaters bull 0 Siamang 10 I

10 20 30 40 50 60

Log Body Weight g

Figure 3 Log life span (years] versus log body weight for the entire set of primate species for which we have data IN = 109 T = 0685 P = 0001 slope = 0172)

of body weight by the residuals method we plotted the base 10 logarithm of the parameter in question (brain weight or life span for example) against the base 10 logshyarithm of the body weight The distance in the y dimension between the least-squares regression line and each data point was added to I giving a valuegt 1 for points that fall above the line and lt1 for points that fall below the line This gives the reshysidual value of this parameter for each speshycies We used the least-squares regression as the basis for calculating residuals beshycause this procedure removes the effect of body weight plotted along the x axis (Harshyvey amp Pagel 1991 We sought to detershynine whether a species that lived longer than one would expect for its body weight had a brain or brain structure that was commensurably larger than would be exshy)ected for its body weight We also used he method of partial correlations to reshyllove the effect of body size on the log-

transformed brain and life span data In virtually every case the partial correlation coefficient was equal to or higher than the residual correlation coefficient (Pearsons r) The advantage of the residuals method is that the distribution of the residuals can be graphed (see Figure 1) The data were analyzed with the assistance of the comshyputer programs Systat and Statview

Brain weight residuals and life span reshysiduals are correlated in haplorhine prishymates (Martin data N = 50 r = 0640 p = lt 0001 Stephan data N = 27 r = 0680 p lt 0001) but not in strepsirhine prishymates (Martin data N = 16 r = 0107 p = 0694 Stephan data N = 13 r = 0272 p = 0369) The distribution of the residuals for brain weight and life span in haplorhine primates reflects dietary specializations In Figure I which plots relative life span against relative brain weight species that are predominately leaf eaters are in the lower-left part of the distribution with

bull bull bull bull

bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull bull

100 A Hakeem G Rodriguez Sandoval M Jones amp J Allmar

smaller brains and shorter life spans speshycies that are predominately fruit eaters are in the middle and upper-right with larger brains and longer life spans the small number of insect eaters are mixed with the fruit eaters the omnivorous human is the extreme upper-right data point The leaf eaters have significantly smaller brains and shorter life spans than the fruit eaters for their body sizes (brains average for 43 frugivores = 1072 average for 9 folivores

C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0

= 0874 P lt OOOli life spans average fOJ 66 frugivores = 1052 average for 17 folio vores = 0811 p = 0007) When the data set is limited to our closest relatives [great apes and humans) the ape with the smallmiddot est brain and shortest life for its body weight the gorilla is a leaf eater which is consistent with the pattern for haplorhine primates as a whole (Allman et al 1993al

Figure 4 shows the correlations for the brain and many of its components as well

tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10

Correlation of Brain Structures and Other Measures with Life Span Residuals

Figure 4 Correlations of brain structures and other measures with life span with the effect of body weight removed for haplorhlne primates The correlation coefficients for the residuals for each brain structure or other measure versus life span residuals are plotted on the scale from -1 to l Correlations that had p values lt005 are represented by stars The structures

3-~~~ gt middottmiddott~l~middotmiddot~lt)~~~~~~r~~~pound~ aaiM~i-i

middot

101FIVE I Brain and Life Span in Primates

as some other measures such as reproducshy tory cortical structures such as the pyshytive maturity BMR pineal volume testes riform lobe IP LOB) prepyriform cortex weight and eye size for haplorhine prishy [PP eER) and the olfactory tubercule (OL mates In each case we calculated the reshy T) are Significantly related to life span siduals relative to body weight as deshy Visual structures such as the eye the scribed above for brain weight relative to lateral geniculate nucleus (LGN) and the body weight and then determined the corshy various measures of primary visual cortex relation with life span residuals relative to (VI 11 VI L26 VI TOT VI WHT) and body weight The structures are plotted in vestibular structures (Ve TOT VC SN descending order of r value from top to botshy ve MN VC IN ve LNJ are not signifishytom The data points represented by stars cantly related Female reproductive matushyare statistically significant at p lt 005 rity (RP AGE) is significantly correlated The data for haplorhines reveal that the with life span but not as well as many brain is a mosaic with respect to life brain structures BMR pineal volume span In haplorhines the most strongly (PIN) and testes size (TESTES) are not sigshycorrelated structure is the cerebellum nificantly correlated ICERBLMJ The second and third most In comparison only two brain strucshystrongly correlated structures are different tures the closely connected globus palshymeasures of neocortical volume (NEO lidus and subthalamus are significantly L26 NEO GY) The fourth structure is the correlated with life span in strepsirhine thalamus (THALM) which is closely conshy primates Reproductive age is not correshynected to the neocortex The amygdala lated with life span when the effect of body and its components (AMYG AM CB AM size is removed in lower primates which

~~

CM) the hypothalamus [HYPO) the subshy is consistent with the lack of correlation stantia innominata (SUB IN] globus palshy between brain or most brain structures lidus tGL PL) and the closely connected and life span The results for one subset of subthalamus (SUBTH) are all well correshy haplorhine primates the catarrhines (Old lated with life span The main and accessoshy World monkeys apes and humans) are ry olfactory bulbs (MOB and AOE) are not very similar to those for haplorhines as a significantly correlated however oHac- whole with a few highly correlated strucshy

~------------------------and other measures are plotted in descending order of correlation from top to bottom AM BC basolateral complex of the amygdala AM CM centromedial complex of the amygdala AM MC magnocellular part of the basolateral amygdala AMYG amygdala AN CO anterior commissure AOB accessory olfactOry bulb BMR basal metabolic rate BRAIN Martin brain weight CER IN interpositus nucleus of the cerebellum CER LN lateral nucleus of the cerebellum CER MN medial nucleus of the cerebellum CER TN cerebellar nuclei total CERBLM cerebellum total OlEN diencephalon EYE surface area of the posterior half of the eye GL PL globus paJlidus HIPPO hippocampus HYPO hypothalamus LGN lateral geniculate nucleus LOT lateral olfactory tract MEOUL medulla MESEN mesencephalon MHN medial habenular nucleus MOB main ollactory bulb NEOCOR neocortex total NEO GY gray matter of the neocortex NEO Ll layer 1 of the neocortex NEO L26 layers 2 through 6 of the neocortex NEO WHT neocortical white matter NTOL nucleus of the lateral olfactory tract OL T olfactory tubercule PIN pineal body P LOB pyriform lobe PP eER prepyriform cortex RETRO retrobulbar cortex RP AGE average female age at first reproduction SEPT seprum STRI striatum SUBCO subcommissural body SUBFO subfomical body SUB IN substantia inshynominata SUBTH subthalamus TELEN telencephalon TESTES testes weight THALM thalamus TRIshyAN triangular nucleus of the septum TRIGM trigeminal complex VC vestibular complex VC IN inferior nucleus of the vestibular complex VC LN lateral nucleus of the vestibular complex VC MN medial nucleus of the vestibular complex VC SN superior nucleus of the vestibular complex VC TOT tOtal vestibular complex VI GR gray matter of the primary visual cortex VI Ll layer 1 of the primary visual cortex VI L26 layers 2 through 6 of primary visual cortex VI TOT total primary visual cortex VI WHT white matter of the Primary visual cortex VPO ventral pons


tures not achieving statistical significance because of small sample size The results for the other subset of haplorhine prishymates the platyrrhines (New World monshykeys reveal that the correlation coeffishycients tend to be lower and only the brain as a whole plus the substantia innomshyinata the cerebellum and the pyriform lobe are significantly related to life span There are 21 structures that are signifishycantly related to life span in catarrhines three in platyrrhines and only two in strepsirhines Finally we considered the more limited set of brain structures for which data are available for humans and the closely related great apes These reshysults are illustrated in Table II whichindishycates very strong correlations between reshysiduals for the brain as a whole and for seven out of the eight brain structures for which data are available Taken together these findings indicate a strong tendency for the brain and its components to beshycome more closely correlated with life span with decreasing phylogenetic disshytance to humans

VI Final Nate

Near the completion of this work we found through an extensive literature search an unpublished doctoral dissertashytion (Witkin 1980) that performed a simishylar analysis of brain and life span in primates using the method of partial corshyrelations on log-transformed data Alshythough the data used in this earlier study were based primarily on published records with maximum life spans that were genershyally shorter than those obtained in the preshysent study (by direct inquiry from zoos and research institutions) many of the conclushysions in Witkin (1980) are similar to those we obtained without knowledge of her study

For example Witkin found that when the effect of body weight was removed for the anthropoidea (monkeys apes and hushy

mans) the partial correlation betweer brain weight and life span was 0617 Using the method of partial correlations tc remove the effect of body weight for the haplorhines [tarsiers monkeys apes and humans) we found a correlation of 0664 for the Martin data and 0714 for the Stephan data However Witkin found a significant partial correlation (0659) beshytween brain and life span for prosimians ilorises lemurs and tarsiers) whereas we did not find significant correlations for strepsirhines (Martin data r == 0175 Steshyphan data r == 0280) This difference is probably due to the considerably shorter life spans used by Witkin for many of the lemurs and by the absence of some lemur species from her longevity data Witkin found that leaf-eating anthropoidea had significantly shorter lives than fruit eatshyers as we have found for the haplorhines Witkin also found that of all the brain structures the neocortex was the best preshydictor of life span in both higher and lower primates We found that the cerebellum was the best predictor in haplorhine prishymates with two measures of neocortical volume being nearly as good predictors in haplorhine primates In strepsirhine prishymates we found only two brain structures that were significantly related to life span the globus pallidus and the subthalamus

Acknowledgments

We thank the 138 zoos and research institushytions who kindly provided primate life span data We especially thank the Duke University Primate Center for longevity data for nine speshycies We thank Prof R D Martin for genershyously providing his unpublished database of body and brain weights We thank Dr Leslie Aiello for providing gut and body weight data We also thankMr ToddMcLaughlin Mr Chrisshytopher Alexander and Ms Prista Charuwom for their valuable assistance in data collecshytion and statistical analysis Support for this research was provided by a grant from the Howshyard Hughes Medical Institute through the Unshydergraduate Biological Sciences Education Proshy

FIVE f Brain and Life Span in Primates

gram and by grants from the National Institute on Aging the McDonnell-Pew Program in Cognitive Neuroscience and the Hixon Proshyfessorship

References

Aiello L amp Wheeler P (1995) The expensive tissue hypothesis The brain and the digesshytive system in human and primate evolution Current Anthropology 36 199-22l

Allman J (1977) Evolution of the visual sys- tern in the early primates Progress in Psy- chobiology and Physiological Psychology 7 1-53

AIJman J (1995) Brain and life span in catarshyrhine primates In R Butler amp J Brody (EdsI Strategies for delaying the dysfunctions of age IPP 221-241) New York Springer

Allman J McLaughlin T amp Hakeem A (1993a) Brain weight and life-span in primate species Proceedings of the National Acadeshy

my of Sciences of the USA 90 118-122 Ulman J McLaughlin T amp Hakeem A

I (l993b) Brain structures and life-span in prishymate species Proceedings of the National Academy of Sciences of the USA 90 3559-3563

Austad S (1993) Retarded senescence in an insular population of Virginia opossums (Dishydelphis virginian a) Tournai of Zoology 229 695-708

Austad S amp Fischer K (1991) Mammalian aging metabolism and ecology Evidence from the bats and marsupials TournaI of Gershyontology Biological Sciences 46 B47-B53

Austad S amp Fischer K (1992) Primate lonshygevity Its place in the mammalian scheme American Journal of Primatology 28 251shy26l

Bacon F (1638) The historie of life and death London Okes

Baron G Frahm H Bhatnagar K Kunwar P ampStepha H il983) Comparison of brain structure volumes in insectivores and prishymates III Main olfactory bulb (MOB) Jourshynal fur Hirnforschung 24 551-568

Chamov E (1991) Evolution of life history variation among female mammals Proceedshyings of the National Academy of Sciences of the USA 88 1134-1137

Chivers D amp Hladik C (1980) Morphology

103

of the gastrointestinal tract in primatesJourshynal of Morphology 166337-386

Clutton-Brock T amp Harvey P (1980) Prishymates brains and ecology Journal of Zooloshygy 190 309-323

Eisenberg J and Wilson D (19781 Relative brain size and feeding strategies in the Chishyroptera Evolution (Lawrence Kans) 32 740-75l

Ershler W Coe c Gravenstein S Schultz K Klopp R Meyer M amp Houser W (1988) Aging and immunity in nonhuman primates L Effects of age and gender on cellushylar immune function in rhesus monkeys (Macaca mulatta) American oumal of Prishymatology 15181-188

Finch C (1990) Longevity senescence and the genome Chicago University of Chicago Press

Frahm H Stephan H amp Baron G (1984) Comparison of brain structure volumes in inshysectivores and primates V Area striataJourshynal fiir Hirnforschung 25 537-557

Frahm H Stephan H amp Stephan M (1982) Comparison of brain structure volumes in inshy

sectivores and primates 1 Neocortex lourshynal fur Hirnforschung 23 375-389

Friedenthal H (19101 Uber die Gultigkeit der Massenwirkung fur der Energieumsatz der lebendigen Substanz Zentral blatt fuer Physioiogie 24 321-327

Goodall J (1986) The chimpanzees of Gombe Cambridge MA Harvard University Press

Harrison R amp Lewis R (1986) The male reshyproductive tract and its fluids In J Erwin (Ed) Comparative primate biology (VoU pp 101-148) New York Alan R Liss

Harvey P Martin R amp Clutton-Brock T (1987) Life histories in comparative perspecshytive In B Smuts D Cheney R Seyfarth R Wrangham amp T Struhsaker (Eds) Primate societies (pp 181-196) Chicago University of Chicago Press

Harvey P amp Pagel M (1991) The comparashytive method in evolutionary biology New York Oxford University Press

Hill K (1993) Life history theory and evolushytionary anthropology Evolutionary Anthroshypology 2 78-88

LindstedtS amp Calder W (1976) Body size and longeVity in birds Condor 78 91-94

MacKinnon J U975) Borneo New York Time-Life Books

104 A Hakecffi C Rodriguez Sandoval M Jones amp J Atln

Martin RjI984J Dwarf and mouse lemurs In D MacDonald (Ed) Encyclopedia of mamshymals (p 331) New York Facts on File

Matano S Baron G Stephan H amp Frahm H (1985) Volume comparisons in the cerebellar complex of primates II Cerebellar nuclei Folia Primatoiogica 44 182-203

Matthews P (1994) The Guinness book of world records New York Bantam

Obituary Annie Lloyd Wei bourn (1992 May 31) Los Angeles Times

Pirlot P amp Stephan H (1970) Encephalizashytions in the chiroptera Canadian Journal of Zoology 48 433-444

Primate life span (1966) International Zoo News 13(61

Promislow D amp Harvey P 1990) Living fast and dying young A comparative analysis of life-history variation among mammals ourshynal of Zoology 220 417-437

Ross C (1988) The intrinsic rate of natural increase and reproductive effort in primates tournai of Zoology 214 199-219

Ross C (1991) Life history patterns of new world monkeys International Journal of Prishymatology 12481-502

Sacher G (1959) Relation of life span to brain weight and body weight in mammals Ciba Foundation Colloquium on AgeingS 115shy133

Smuts B Cheney D Seyfarth R Wrangham R amp Struhsaker T (1987) Primate socishyeties Chicago University of Chicago Press

Stephan H Baron G amp Frahm H (1982)

Comparison of brain structure volumes in sectivores and primates II Accessory olf tory bulb (AOB) Journal filr HirnforschUl 23 575-591

Stephan H Frahm H amp Baron G (198 New and revised data on volumes of bra structures in insectivores and primates Fol Primawlogica 35 1-29

Stephan H Frahm H amp Baron G 1198 Comparison of brain structure volumes in i sectivores and primates IV Non-cortical v sual structures tournai filr Hirnforschun 25385-403

Stephan H Frahm H amp Baron G (1987 Comparison of brain structure volumes in iI sectivora and primates VII Amygdaloi components Journal filr Hirnforschung 2c 571- 584

Stephan H Nelson J amp Frahm H (1981) Brain size comparison in chiroptera Zeitschrift filr Zoologische Systematik unc Evolutionsforschung 19 195-222

Tigges J Gordon T McClure H Hall E amp Peters A (1988) Survival rate and life span at the Yerkes Primate Research Center American ournal of Primatology IS 263shy273

Witkin J (1980) Primate brain and life histoshyry Unpublished doctoral dissertation Coshylumbia University New York

Zihlman A Morbeck M ampGoodallJ (19901 Skeletal biology and individual life history of Gombe chimpanzees Journal of Zoology 22137-61


about the same Kenneth Glander (personshyal communication February 1 1993) has measured tooth wear in a wild population of 580 howler monkeys Alouatta palliata) in Costa Rica since 1970 Twelve of these monkeys have been under observation since 1970 In these old monkeys the teeth are all worn down to the gum line He estimates them to be between 24 and 28 years old The maximum life spans reshycorded for captive Alouatta species range from 20-25 years and thus appear tole fairly close to their longevity in the wild

Goodall (1986) observed 11 chimpanshyzees that she considered old at Gombe from 1965 through 1983 One of these was Flo who was a very successful individual with high-ranking offspring Figan and Fifi Flos teeth were worn down to the gum line and Goodall estimated her age four years before her death as II certainly more than 40 (p 104 see also Zihlman Morbeck amp Goodall 1990) Flos status and aggressive personality were strong facshytors in Figan and Pifis achievement of high rank Flo remained reproductive into old age but her last two offspring Flint and Flame did not flourish The infant Flame died during her motherS illness Flint although more than 8 years old at the time of his motherS death was unable to survive without her support For 8 years at Ranoinafana in Madagascar Patricia Wright (personal communication March 1 1993) observed a dominant female Proshypithecus diadema th~t she estimated on the basis of extreme tooth wear to be close to 30 years of age at the time of her death

Thus the limited data available from prishymates living in natural conditions indicate hat some individuals live into robust old

age Goodalls observations of Flo and her family also suggest that a parents longevishyty contributes to the success of the offshyspring even as adults and is likely to be a factor in the evolution of life spanshySustaining mechanisms in higher prishymates The parents longevity may be particularly important in catarrhine prishy

79

mates and especially in apes and humans because development is slow the period of dependence on the parents is long and even in adulthood the success of the offshyspring may be closely linked to parental status Because of late reproductive age long interbirth intervals and long periods of dependence on the mother female apes must live more than half the maximum reported life span for these species to maintain the population at the stable reshyplacement level (Goodall 1986 Ross 1991 Smuts Cheney Seyfarth Wranshygham amp Struhsaker 1987 see Table I) These factors may be responsible in part for the strong correlations between brain (and most brain structures) and life span in the group made up of gorillas orangutans chimpanzees and humans (see Table II) The selective pressure for maternal lonshygevity may also explain the predominance of females in our sample of very old prishy

~mates (Table I) and the much lower female mortality rates in contemporary human populations

III Brains Life Span and Diet

We have confirmed earlier studies that fruit-eating primates have significantly larger brains than leaf-eating primates (Clutton-Brock amp Harvey 1980) Fruitshyeating bats also have larger brains for their body size than insect eaters (Eisenberg amp Wilson 1978 PirIot amp Stephan 1970 Steshyphan Nelson amp Frahm 1981) A fruit eatshyers food supply is not constant because different plants bear fruit at different times and at different locations in the complex matrix of the tropical forest (MacKinnon 1975) An animal guided by memory of the locations of fruit-bearing trees can more efficiently exploit the available fruit resources than would othershywise be possible thus natural selection may have favored the development of cashypacities for visuospatial memory in frushygivorous primates (Allman 1977) This

--~ --- --------------------

















California



















(continuesl

r

Thble I


























00 (JJ


Cercopithecus diana


Cercopithecus diana


Cercopithecus mitis

Cercopithecus mitis

Cercopitheclls muna

2050

1470 L

3160 L

3100

2300 L

2825 2592 2500 L

2300 L

2300 L

3725

480

3000 L

2700

2710 L

2500 L

2200

47

13 C

4

25 2233

2

33)

333

5

21

417

71611

411174

21872

811458 43084 519155

1212272

1212272

11140

2466

912980

6121166

1112171

U

f

M Aba

U

M Jonathan

1212485 12887

F F F

F

Nosy

M

U

U

F Dora

711185 M

F

F

Sarah 192

U

f

















Ross (1991) 2591

kontinues)

Table I










1617 L 2410 L

4 17

228179 6684

F F


61191 611191





Zoo Illinois














(Xl










(continues)

1

DIble I Continued)

















lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103






































--~ --- --------------------

















California



















(continuesl

r

Thble I


























00 (JJ


Cercopithecus diana


Cercopithecus diana


Cercopithecus mitis

Cercopithecus mitis

Cercopitheclls muna

2050

1470 L

3160 L

3100

2300 L

2825 2592 2500 L

2300 L

2300 L

3725

480

3000 L

2700

2710 L

2500 L

2200

47

13 C

4

25 2233

2

33)

333

5

21

417

71611

411174

21872

811458 43084 519155

1212272

1212272

11140

2466

912980

6121166

1112171

U

f

M Aba

U

M Jonathan

1212485 12887

F F F

F

Nosy

M

U

U

F Dora

711185 M

F

F

Sarah 192

U

f

















Ross (1991) 2591

kontinues)

Table I










1617 L 2410 L

4 17

228179 6684

F F


61191 611191





Zoo Illinois














(Xl










(continues)

1

DIble I Continued)

















lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103























































(continuesl

r

Thble I


























00 (JJ


Cercopithecus diana


Cercopithecus diana


Cercopithecus mitis

Cercopithecus mitis

Cercopitheclls muna

2050

1470 L

3160 L

3100

2300 L

2825 2592 2500 L

2300 L

2300 L

3725

480

3000 L

2700

2710 L

2500 L

2200

47

13 C

4

25 2233

2

33)

333

5

21

417

71611

411174

21872

811458 43084 519155

1212272

1212272

11140

2466

912980

6121166

1112171

U

f

M Aba

U

M Jonathan

1212485 12887

F F F

F

Nosy

M

U

U

F Dora

711185 M

F

F

Sarah 192

U

f

















Ross (1991) 2591

kontinues)

Table I










1617 L 2410 L

4 17

228179 6684

F F


61191 611191





Zoo Illinois














(Xl










(continues)

1

DIble I Continued)

















lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103






































Thble I


























00 (JJ


Cercopithecus diana


Cercopithecus diana


Cercopithecus mitis

Cercopithecus mitis

Cercopitheclls muna

2050

1470 L

3160 L

3100

2300 L

2825 2592 2500 L

2300 L

2300 L

3725

480

3000 L

2700

2710 L

2500 L

2200

47

13 C

4

25 2233

2

33)

333

5

21

417

71611

411174

21872

811458 43084 519155

1212272

1212272

11140

2466

912980

6121166

1112171

U

f

M Aba

U

M Jonathan

1212485 12887

F F F

F

Nosy

M

U

U

F Dora

711185 M

F

F

Sarah 192

U

f

















Ross (1991) 2591

kontinues)

Table I










1617 L 2410 L

4 17

228179 6684

F F


61191 611191





Zoo Illinois














(Xl










(continues)

1

DIble I Continued)

















lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103













































00 (JJ


Cercopithecus diana


Cercopithecus diana


Cercopithecus mitis

Cercopithecus mitis

Cercopitheclls muna

2050

1470 L

3160 L

3100

2300 L

2825 2592 2500 L

2300 L

2300 L

3725

480

3000 L

2700

2710 L

2500 L

2200

47

13 C

4

25 2233

2

33)

333

5

21

417

71611

411174

21872

811458 43084 519155

1212272

1212272

11140

2466

912980

6121166

1112171

U

f

M Aba

U

M Jonathan

1212485 12887

F F F

F

Nosy

M

U

U

F Dora

711185 M

F

F

Sarah 192

U

f

















Ross (1991) 2591

kontinues)

Table I










1617 L 2410 L

4 17

228179 6684

F F


61191 611191





Zoo Illinois














(Xl










(continues)

1

DIble I Continued)

















lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103






































Table I










1617 L 2410 L

4 17

228179 6684

F F


61191 611191





Zoo Illinois














(Xl










(continues)

1

DIble I Continued)

















lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103













































(Xl










(continues)

1

DIble I Continued)

















lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103






































DIble I Continued)

















lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103






































lIyubales llWcXJI


muelleri


Hylobales pileatus







Lemur calta

Lemur catta

Lemur catta


Lemur fulvus


290() L

2500 L

2500 L

3600

310f) L 3792

3800 L

3700

1000

2590 2475

3000 L

2710

2-600 L

1842 3700

3650

2800 2710

3

3

8

2 C

6

7

45

3

225 C

25

C

7164

7lJ69

71169

7163

41962 10244

M3160

72059

Iliol

1111051

7265

9486

102505 8310

III 58

81154

9991

9382

32389

3787

81577

2l46

5492

73182

--_1

M

F

Smiler

Berta 690701

F Gibby 690702

M

M F

Simon

Boston Blackie

F

M

Suzy

F

U M

Lulu

F

U

U

U M

F Yvette 52lf

F U



















(continues)

-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103






































-- -----~~------- _w4~o~--~~~--~_____









2425 3200 L 2 61262

U F Saturna 524f


Center Durham North








2200 1640

622164 619174

8111186 1112489

F M


121086 85192




3000 3000

U U


25191




2008 L 1710 UOI

3B 61175

jUB1 gt111171

F lJ II

Mandy 66 Maryland


BillY I 25191


















(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103























































(continues)

ltr

Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103






































Iable I








garnetti many




























(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103
























































(continues)

1


Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103







































Idble I Continued)








QN


























T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103





















































T




Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103









































Brain structure r p









15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103







































15

14

13

l 12

c= I

11CB ~ 10= c= c

09JJ

~ l 08

07

06

05

bull o

bull


q

bull

bullbull

bull


95

05 06 07 08 09 10 11 12 13 14 15






and Mammals














97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103


















































97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103










































97








40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103









































40

30

l)I


j 10

00 10 20 30




40 50 60

Log Body Weight g



22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103







































22

20 +

18 bulli

bullQgt

16C rI


+ Homo sapiens OIl

oS 0 Insect Eaters



10 20 30 40 50 60

Log Body Weight g





bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103






































bull bull bull bull




C~RBLMN OL26

tt~~E~ PL8BAM B

NEOL1 SUB IN AMYG

NEOWHT BRAIN

_LPL NEOCOR

PPCER RPAGE CERIM

ST I AMCM MES~N

DI N OLT VPO

_ SN VI L1

V1 L26 MEDUL AN CO

VbOTMN PIN

H1p9gt8VLGR

V1TOT RETRO

LGN VIWH~

BM VCTOT

MHN MO B

CERMN TESTES

EYE CERIN VC~N

SUB 0



tl

f

) It

t

bull

I -10

I -05

I 00

I 05

I 10




middot



~~





VI Final Nate




Acknowledgments




References














103







































middot



~~





VI Final Nate




Acknowledgments




References














103








































VI Final Nate




Acknowledgments




References














103








































References














103



























































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