Systematics and body size: implications for feeding adaptations in New World monkeys.

AMERICAN JOURNAL, OF PHYSICAL ANTHROPOLOGY 88:415468 (1992)

Systematics and Body Size: Implications for Feeding Adaptations in New World Monkeys SUSAN M. FORD AND LESA C. DAVIS Department of Anthropology, Southern Illinois Uniuersity, Carbondale, Illinois 62901

KEY WORDS Platyrrhines, Body size, Systematics, Feeding ecology, Sexual dimorphism, Cope’s Law ABSTRACT The relationship between body size and feeding ecology is well established for primates. It is argued that the evolutionary history of modern New World monkeys and, in particular, the path to attainment of current body size is significant in understanding the similarities and differences between dietary strategies and other ecological parameters of similarsized monkeys. Current interpretations of New World monkey evolutionary relationships are reviewed. Based on a synthesis of available body weights and the assumption that the earliest New World monkeys weighed close to 1 kg, similar to modern Aotus and Callicebus, predicted patterns of body size change in each lineage are given. Restrictions on directions of body size change in primates are discussed, and it is shown that “Stanley’sRule” offers a good explanation for differing body size ranges in New and Old World anthropoids. Predicted ecological correlates to body size drawn from the mammalian literature are offered and tested using data on New World monkeys, which show some concurrence and several interesting departures from predicted patterns. Sexual dimorphism in body weight of New World monkey species is reviewed, based on the new summary of body weight data given. 0 1992 Wiley-Liss, Inc. Among the morphological traits that influence animal foraging capacities, body size has the most pervasive effect. (Temerin et al., 1984, pg. 215) It i s , . , appropriate to view the evolution of body size, whatever its selective basis, as inextricably involved with the evolution of foraging strategies. (ibid., pg. 241)

The basic relationship between body size and dietary strategy has been well established in primates as a group. In general, the quality of the diet and the use of animal (including insect) prey decreases as body size increases (e.g., Gaulin, 1979; Gaulin and Konner, 1977; Kay, 1984; Sailer et al., 1985; Temerin et al., 1984; Terborgh, 1983, 1985). Body size constrains not only food type but also choice of concentrated vs. dispersed food items, techniques of prey search and capture, and use of space including vertical position in forest strata, choice of habitat, and locomotor specializations (Eisenberg, 0 1992 WILEY-LISS, INC.

1981,1990;Fleagle, 1988;Fleagle and Mittermeier, 1980;Martin, 1990;Terborgh, 1985). However, different adaptations within a broad feeding category develop, and primates of the same body size can exhibit strikingly diverse foraging strategies, especially in the Neotropics (Terborgh, 1985). These may in part result from primates attaining a similar body size via separate evolutionary pathways. Any study or symposium, such as this, which is interested in the ~

Received July 11,1990; accepted January 27,1992

416

S.M. FORD AND L.C. DAVIS

Cronin (1980), and in the frequently used classification of Thorington and Anderson (1984). Diverse studies on New World monkey relationships over the last decade indicate that the marmosets and tamarins are neither the most primitive group nor the sistergroup to all other New World monkeys, but have their closest relationship to some other members of the New World monkey clade; this renders the “Cebidae”of common usage a polyphyletic group. Therefore, the classic division of CebidaeJCallitrichidae is inaccurate, and continued adherence to it and the associated groupings obscures true relationships. Once this basic premise is accepted, various closer relationships between different groups should become clearer. However, major disagreements currently exist over precisely which non-clawed New World monkeys are in fact most closely related to the clawed marmosets and tamarins. The purpose here is to provide a framework for looking at changes in body size through time. It is not our intention, nor would it be possible in any brief space, to review all of the data used to support or refute one or another of the systematic arrangements favored by current authors, the most recent systematic revisions being offered by Rosenberger (1979, 1981; Rosenberger et al., 19901 and Ford (1980, 1986), along with partial revisions by Baba et al. (19801, Dunlap et al. (19851, Kay (1989, 1990a1,and Dickinson et al. (1989).The data OVERVIEW OF NEW WORLD MONKEY are many and varied: Hershkovitz’ (1977 PHYLOGENY: ALTERNATE VIEWS and elsewhere) view is based on a somewhat Until the last decade, almost all discus- eclectic choice of a varying number of traits; sions of the overall evolutionary relation- Sarich and Cronin’s (1980) work on immuships of New World monkeys emphasized a nological data; Rosenberger’s (1979, 1981; basic dichotomy between the small, clawed, Rosenberger et al., 1990) on a more clearly two-molared marmosets and tamarins, gen- defined set of over one hundred primarily erally referred to as the callitrichids, and dental features, but including a few other the remaining genera, generally lumped as miscellaneous features; Ford’s (1986) on the cebids. The latter group was usually con- Rosenberger’s cranial and dental data plus sidered to consist of many separate and an- nearly one hundred postcranial features, cient lineages, of unclear relationship to one and several other attributes such as karyoanother except in a few cases. The most au- types; Baba et al.’s (1980) on ouchterlony thoritative proponent of this general view, data; Dunlap et al.’s (1985) on forelimb myhereafter referred to as the “classic”taxon- ology; Kay’s (1990a) study on 165 dental feaomy, was and remains Hershkovitz (1977 tures, the data having been collected indeand elsewhere), but it was basically mir- pendently of Rosenberger’s data; and rored by the molecular studies of Sarich and Dickinson et al.’s (1989) study is based on

evolution of feeding strategies must consider not only the current body size of the animals in question, but also the evolutionary history of the development of that size and whether it was attained in concert with or convergent upon other closely related animals of similar size. This requires an understanding of both the phylogenetic relationships of the group and the patterns of body size change through time in its various lineages. Recent studies have led to a clearer understanding of New World monkey systematics, although there remain areas of disagreement or confusion. As a baseline for this symposium, current views on the evolutionary relationships of New World monkeys are reviewed here. A compendium of published original body weight data for New World monkeys (Tables 1 and 2) is then used as a data base to explore directions of changes in body size in the evolution of New World monkey lineages. This “evolutionary perspective” on body size forms the basis for: 1) an investigation into constraints on body size in primates and the possible causes of the release of those constraints in certain groups; 2) a test of predicted associations of ecological parameters with body size in New World monkeys; and 3) a brief overview of patterns of sexual dimorphism in body weight in New World monkeys.

CHANGES IN PLATYRRHINE BODY SIZE

417

Fig. 1. “Classic” systematic arrangement of New World monkeys. This cladogram is modified from Sarich and Cronin (19801, but largely mirrors the view of Hershkovitz (1977) and others (see text).

two-dimensional electrophoresis (2DE). Other earlier work based largely on single or a few attributes are not reviewed separately here; much of these data were incorporated in the larger data set analyzed by Ford (1986). This includes, for example, analyses based on dental eruption sequences (Byrd, 1981),karyotypes (Chiarelli, 1980; De Boer, 1974), nose shape (Maier, 19801, and brain structure (Falk, 1979,1980). No particular systematic arrangement will be favored here, although clearly we have biases. The most widely used andlor most recent alternatives will each be briefly outlined along with the underlying principles or techniques that guided their construction. Major areas of agreement and disagreement between these views will be highlighted. Then we will concentrate on what we interpret to be the patterns and directions of body size change, given each view of New World monkey relationships.

As will be clear, there are far more points of agreement than disagreement. The arrangement shown in Figure 1,drawn from the work of Sarich and Cronin (19801, is based on a quantitative evaluation of molecular data. It in fact represents a variant of the taxonomic scheme favored by Hershkovitz (1977). Hershkovitz based his systematic arrangement on an overriding principle of increase in body size through time. This results in the separation of the small, clawed marmosets and tamarins from all other New World monkeys, leaving multiple unresolved divergences within his family Cebidae, the larger, non-clawed genera plus Callimico. This is the “classic” dichotomous division of the New World monkeys. Rosenberger’s systematic view (1979, 1981;Rosenberger et al., 1990,1992), shown in Figure 2, is based on a very different overriding principle, one that is appropriate to consider within the context of this sympo-

418


Fig. 2. Systematic arrangement of New World monkeys according to Rosenberger, modified from Rosenberger (1981).

sium. He argues that major adaptive zones, as defined primarily by dietary and feeding strategies, were invaded only once during the New World monkey radiation, with subsequent specialization within these zones. Thus, he separates the basic frugivoreinsectivores (the marmosets and tamarins, including Callimico, plus Saimiri and Cebus) from the frugivore-folivores(a less easily defined group, including the atelines, the saki-uakaris, Callicebus, and Aotus). Within the frugivore-insectivore group, the clawed marmosets and tamarins remain a clear and strong unit, sharing many traits, and the omnivorous Cebus and Saimiri are closely related to one another. Among the frugivorefolivores, the large and more suspensory atelines are closely related, as in all systematic arrangements, with Alouatta being the closest relative of this group and sharing their prehensile tail, large size, and many other traits. The poorly known saki-uakaris

are closely related to one another, and in Rosenberger’sview, Callicebus (the monogamous titi monkeys) and Aotus (the monogamous, nocturnal night monkeys) are most closely related to the saki-uakaris. Rosenberger continues to support this grouping of his Pitheciinae, albeit with some alteration in the relative positions ofAotus and Callicebus (1984, 1992; Rosenberger et al., 1990). However, Wright (1989) found that Aotus spends 20% of its time foraging for insects, which represent a larger portion of its diet compared to that of Callicebus. Indeed, she found that during the dry season, Aotus shifts to a diet primarily of nectar, figs, and insects. Based on her work, Terborgh (1985) suggested that the diet of Aotus is in fact highly omnivorous and strikingly similar to that of Saimiri, the squirrel monkey. Its placement in the frugivore-folivore group is difficult to defend given these data on Aotus’ diet.


419

Fig. 3. Systematic arrangement of New World monkeys according t o Ford, modified from Ford (1986).

Ford’s (1986, see also 1980) view of New one another; the large, prehensile-tailed World monkey relationships, shown in atelines with each other and with Alouatta; Figure 3, is based on a larger, more varied and the three extant saki-uakari genera to data base but also on yet a third principle. one another. These two schemes also agree She used a form of “numerical cladistics” an- on the relatively close relationship between alyzing data from many different functional the saki-uakari group and the atelines. areas, rather than a single adaptive com- Ford’s view differs primarily in the placeplex, to seek a best solution. While this ap- ment of four genera. Rather than aligning proach assumes that parsimony is at Aotus and Callicebus with the saki-uakaris, present our best tool for beginning to sort and Cebus and Saimiri with each other and out systematic relationships, evolution has the marmosets and tamarins, Ford suggests repeatedly demonstrated itself to be less that these four are the result of lines divergthan perfectly parsimonious. Convergences ing much earlier in the history of New World (in body size, dietary strategies, locomotor monkeys. Aotus and Callicebus would aptype) and reversals have occurred repeat- pear to be most closely related to each other, edly. Therefore, Ford also considered the although distinctive in a number of ways. nature of the features examined and their Saimiri is most likely a distant sister-taxon relative likelihood of developing homoplasti- to these two, although a reasonable alternacally, using several criteria. Ford’s resulting tive interpretation could suggest that Cecladogram agrees with that of Rosenberger bus, rather than being the sister-taxon to all in the close ties of: the small, clawed marmo- other New World monkeys, is actually most sets and tamarins, including Callimico, to closely related to Saimiri. In either case, Ce-

420


Fig. 4. Systematic arrangement of New World monkeys according to Kay, modified from Kay (1990a) (Kay [1990a] does not give family and subfamily names).

bus has diverged considerably from all other New World monkeys and has converged in various features on several different lineages, further obscuring its phylogeneticties. Dunlap et al. (1985) have also done a numerical cladistic analysis, based on data on variation in 19 muscles in the forelimb. Their sample did not include any sakiuakaris or Brachyteles. They do not offer a single best systematic arrangement, but discuss several that appear to be strongly supported by their data. These largely agree with Ford’s view, with the most notable exception being the place of Aotus. Aotus appears to have strong, derived similarities to the forelimb myology of the atelines (includingAlouatta). Given the absence of the sakiuakaris from this study, this placement of Aotus is similar to that suggested by Rosenberger, except that Callicebus is definitely excluded from this group. In Dunlap et al.’s study, Saimiri could be interpreted as hav-

ing ties to this Aotuslateline group, or as being more primitive, along with Cebus and Callicebus. However, neither Saimiri nor Cebus appear to have affinities to the marmosetltamarin group (in contrast to Rosenberger’sview). Kay’s current (1989, 1990a) work, shown in Figure 4, is based on a very similar approach to Ford’s, although using slightly different numerical techniques and somewhat different criteria for determining primitive character states. It is also based exclusively on dental data. Kay found, as did Ford, that numerous homoplasies and reversals have characterized New World monkey evolution. As with most other studies, Kay finds that the small marmosets and tamarins plus Callimico, the saki-uakaris, and the large atelines plus Alouatta form three distinct groups. In addition, Kay’s study supports Rosenberger’sview that Saimiri (but not Cebus) has close ties to the marmosets and


tamarins, but supports Ford’s suggestion that Cebus and Callicebus form two separate out-groups to all other New World monkeys (although with Callicebus an earlier offshoot than Cebus). However, there are several key differences suggested by Kay. One is that Brachyteles may be closest to Alouattu among the large, prehensile-tailed forms (Ford indicates affinities to either Ateles or Lagothrix; virtually all others affine Bruchyteles with Ateles). Another is that the saki-uakaris are a very unique group lacking strong affinities to any other extant New World monkey group, reminiscent of the “classic” view. And Aotus also lacks strong ties-either to Callicebus (as in Ford and some versions of the “classic” view), the saki-uakaris (as in Rosenberger), or the atelines (as in Dunlap et al.). Kay figures a trichotomy of the small marmosets and tamarins (including Callimico), the large atelines, and Aotus, but he suggests numerous alterations of this view are possible, some incorporating closer ties of one or another of these clades to Callicebus or Cebus. Dickinson et al. (1989) are working on a cladistic analysis of New World monkeys, using the innovative technique of twodimensional electrophoresis (2DE), analyzing the data cladistically. Their preliminary results examining Saguinus, Saimiri, and Ateles supports Rosenberger’s and Kay’s suggestions that Saimiri is closer to the marmosets and tamarins than it is to atelines. However, their work has not yet incorporated Cebus or the remaining platyrrhines. It is clear that the affinities of Cebus, Saimiri, Aotus, and Callicebus to one another and to the other New World monkeys remains the major area of controversy in platyrrhine systematics, and that this issue is far from resolved to anyone’s satisfaction.

421

discussion is accurate information on the body size of extant New World monkeys. Here, we use body weight as a measure of body size. Body weight is commonly used as an indicator of overall body size, and it is particularly relevant when one is concerned with diet and feeding ecology, the subject of this issue. Many different and widely varying values for body weight are given in recent literature, frequently drawn from other sources. Table 1 presents all of the original data we could trace on body weights for New World monkeys, with the sources listed in Table 2 (see also Appendix A). No secondary sources are included unless noted, and only data on healthy, adult animals are listed. Data for both wild-caught and captive animals are given, with that on wild-caught animals in boldface. Mean values are given in Table 3. Means of wild-caught specimens (combined sex) are used as the basis of the following discussion (except as noted in Table 3). The issue of sexual dimorphism in New World monkeys is discussed below. Any discussion of changes in body size must begin with an assumption of the ancestral body size for New Worldmonkeys. Hershkovitz (1977, as well as views derived directly from his view), by virtue of his assumption that no evolutionary size decrease is possible, suggests that Cebuella is the most primitive, and that all other genera have arisen from this genus as a result of increases in body size. Most other analyses suggest that the earliest New World monkey was similar in body size as well as many (but certainly not all) aspects of structure to Aotus and/or Callicebus (Dunlap et al., 1985; Ford, 1980, 1986; Kay, 1980, 1990a; Rose and Fleagle, 1981). These monkeys weigh close to 1 kg (Aotus is 902 g, Callicebus is 1,005 g). Saimiri has also been suggested as being close to the primitive New World monkey in many features, possibly including EVOLUTION OF BODY SIZE body size (most recently by Kay, 1989; see The crucial issue for this paper is the also Rose and Fleagle, 1981); it is slightly likely pattern and directions of body size smaller in body size, with a mean of 836 g. change in the lineages leading to the extant The earliest known fossil New World monNeotropical primates. While some differ- key, Brunisella from Salla, Bolivia, was ences arise depending on which taxonomic probably similar to Aotus in body size, possiview one favors, there is remarkable congru- bly around 1 kg (Fleagle, 1988), although ence on a number of points. Central to this Rosenberger et al. (1990) gave a somewhat

SP. argentata

Callithrir

jacchus

humeralifer

aurita emiliae flauiceps geoffroyi

Species

Genus

humeralifer

subsp.

argentata

subsp.

Subspecies

(14) (4)

107-125 145- 190

('9

(8 (1)

360

(1)

(3)

(?)

(40)

(5)

300-349 346-375 350 134-300

200-310 206 306

(4)

232-376 256-381

261-293 375-387 350-617 125-287 300-400 300

240-300 236

380

190

(3)

230-350 360

260-400

(12)

126-141 100-155

Female weights

230-390

330 380 300-413

(4

Male weights

TABLE 1. New World monkey body weights' (n)

270-350 295-393 330 336 250-350

200-310

248 310

380

406 320 359

429

250-600

100 125 100 100

Sex unknown weights (n)

89' 904 89' 103 108 103 7 102~ 89' 1g4 904 103 604110 46" 30 74 8" 61 30 73 129 76 16 333 7g13 80 68

111

1g4 39 7 29 log4 1216 1277 465 15 11g4 7

1014.5

1173

Source'

Saguinus

520 272-395 529 450 600 264-350 320

490 330 595-907 500-600 510-650

264 3 10-4 10

subsp. midas

niger

380-495 495 515

397-505 491 477

labiatus

leucopus midas

550

490

340-415 327-535 415 270-400 505-545 597 640 453-567 448-558

338-429

430 370

subsp.

(3) (4)

labiatus

320-388 365-483 405 290-420 482 631 660 510 432-532 486

389-436

430 420

182

subsp.

weddelli

fuscicollis illigeri nigrifrons

subsp.

225

imperator

geoffroyi

bicolor fuscicollis

SP.

kuhli penicillata

(4) (4)

.

(?)

400-550 350-500

383

570

533

500-650 440

110

974 102~ 7 103 53

1155

102~ 13 128

1014.5

1216 1277

log1* 53 103 log4 29 7 7 121-5 1277 974 101~~~ log4 102~ 103 4611 333 16 1163,'5 1163*15 1163,'5 41 128 898 92 113 112 5716 223J7 46 2718 70

86 58 (1) 6O4,l0 53 8l2 (3) 15 (continued)

(16)

(?) (?) ..

(1)

(?)

(?) (?)

520

I

(19) (13)

(?)

(471

(3) (3)

(?)

(71)

(?)

(?) (?)

(?) (?)

(12)

(?)

800 650

330-436 340-400 305-361 265-321

400 250-400 300-400 362 410 364 367

340 490 400

375

Zeontopithecus

Genus

subsp.

mystax

chrysomelas chrysop gus rosalia2 J

hernandezi subsp."

oedipus

oedipus

subsp.

nigricollis

mystax

Subspecies

Species

360 540-700 540-690 611-777 437-627 710

390-471 431-473 490 553 450-560 550

588-794 546-654 361-665 630

480-590

540-623

745

412-461 481 480 410-555

500 380-480 244-300 394 440 510

(3

450-482

(6) (4)

458-505

(3

350-430 348-413 417 573

633 490-561 468-652 460

(5) (161) (16)

508-640 511-556

Female weights

639 472-525 503-681 470

(30) (2)

(4

493-643 491-510

Male weights

TABLE 1 . New World monkey body weights' (continued)

(1) (15) (3)

(?)

(3

(104) (5) (11)

(4

600-800

650-750

450-550 460-650

293

360-450 270

360 350

460

Sex unknown weights

(?)

(?)

(12)

(?)

(8)

(?)

(?)

(?)

(5)

(n)

18 1 65

461'

104 104 56

4

30

444

644,5

108

63 53 104

461'

16 120 46

6723 -.

1022

16 118 47 94

46'1

41 7 102~ 374,5

$9

103

Source'

Aotus

fip.28

~aimiri'~

sci~reus~~

azarae lemurinus

SP.

ustus ~anzolinii~~

oerstedi subsp.

subsp. griseimembra lemurinus

sciureus

subsp.

peruuiensis

boliuiensis

subsp.

oerstedi

boliuiensis

goeldii

Callimico

889 1,020

554 1,150 620-1,200 950 825-1,020

1,000- 1,250 746-812 710 967 407-630 720 727-810 1,134 471-930 715-937 800-1.000

930-950 893 890 750 907 1,000 625-830 1,052 960 910 800 715

1,300-1,600 1,100 963-1.088

400-535 725

278

(2) (1) (8) (9) (2)

(6)

(3

(6) (5) (10) (3) (1) (7)

(2)

651 1,250 710-880 650 1,249 780

530-710 480-620

681 327-345 570 497-611 491-756

540-750 775 790

900-1,270

547-887 710

680

1,000 722

607

1.000

500 410-555

26 12 933 143 (76) (9) 118 54 58% 898 7 9138 54 66 (6) 21 113 112 (continued)

2435

12V 103 1729 823 86 813' 8'2 8l2 9633 20 934

253'

7 2529

604,'0

21 1216 36 110

1i3I

53 1216 72 7lZ6 29 1729 8g8 12430 2 49 113 112

Callicebus

Genus

torquatus

personatus

donacophilis hoffmannsi moloch

cupreus

brunneus

SP.

nancymai

Species

1,100

1,500

1,950 1,050-1,650 700

nigrifrons personatus

subsp. lucifer lugens medemi

1,100-1,600

1,200 670

800

1,080 850-1,200 840

845 748-960 1,000-1,175 845-1,010 1,178 800

681

825-1,025

920

567-1.208

1,200-1,450 1,151-1,462

970-1,600

1,370

1,266

920 990 700-1,020

1,075 1,163

850 760-850

715-1,120 560-1,ooO

900-1.000 930

690-1,232

Female weights

780-1,100 780 808-928

(14)

(n)

825-1,050 795 861-980

Male weights

melanochir

cupreus discolor ornatus pallescens subsp.

triuirgatus

subsp.

Subspecies

TABLE 1. New World monkey body weights' (continued)

1,121

Sex unknown weights

(14)

(n)

52 898 111 1216 374*5 127' 103 10i5 8'2 108 52 108 52 108 103 52 85 52

7

54 624 29 9141 52 898 52 52 52 52 898

812

48 5 783,39.40 7740 64435 7 604~0 1216 1277 103 2718 28

Source2

Cacajao

Chiropotes

Pithecia

964-1,685 1,650-2,500

pithecia

SP.

caluus melanocephalus

satanas

2,510 4,100 3,450

2,200-4,000 2,200-4,000 2,230-4,000 3,500 2,800-3,100 2,770-3,130

3,000 2,500 3,550 2,880 2,740

2,000-3,300 2,000-3,300 1,900-2,950 2,500

2,660

2,880

satanas

chiropotes

2,220-2.720 2,220-2,720 2,800 2,520

779-1,100 1,550-1,750 964

1,980-2,160 1,100-2,650 2,170 2,177 1,300-1,500 2,000-2,500 1,260-1,770 1,347 1,530 1,512 2,250 1,510

2,950-3,320 2.903-3.320 2;720-3;000 3,170 subsp.

1,650-2,500 1,380- 1,760 1,770-1,910 1,447-1,701 1,750-2,100 1,800 1,750-2,100

subsp.

2,920 1,100-2,750 2.490 2,600-2.800 2,500-3,100

- 7 -

xnnn --

albinasus

SP.

pithecia

subsp.

monachus milleri monachus

irrorata

SP.

albicans irrorata

2,975

2,482 2,980 2,800

2,800

3.000

1,800

1,500

7

7

87 504 34

36

6

504.44 89' 58 86

103 604," 594,5

7

89' 7 5g4,5

504,43

103 (continued)

(8)

(17) (4) (?)

(?)

(?)

(4)

7 58 6O4,'' 54 89' 5443 29 6

86

51 51 514 .~ 95 51 36 110

7

51 8g8

SP.

Cebus

olivaceous

capucinus

apella

albifrons

Species

Genus

linnae~s~~

subsp.

lus) libidinosus f= cay) robustus xanthosternos

(= macrocepha-

apella

subsp.

Subspecies

3,180-5,450 3,833 1,447-3,007 4,500 4,250

2,300 3,110-3,320 3.200 1,300-1,470 2,300 3,970 3,765

2,900

3,180-4,090 2,718 1,589 3,200

2,610 2,722

1,770

3,000 3,100

1,774-1,856

2,314-2,462 1,362-2,156 3,900-4,800 4,500 3,300-3,800 1,900

1,400-1,730

2,228 2,220

Female weights

2,500 1,940 1,370-3,400 2,450 1,758

(n)

3,300 3.330 1,350-4,250 3,370

2,200

2,430-2,755 2,650 3,260 1,700

Male weights

TABLE 1. New World monkey body weights' (continued) (n)

3,101

2,600

1,500-3,500 3,000 3,000 2,110

1,500-3,500 2.800 2;500 2,428 2,300-2,520

2,500-4,000

Sex unknown weights (n)

108 54 108 54 108 112 113 27" 35 21 54 865 58 36

58 86 54

loo4 45 23 604.10 89' 12645 7 127' 1216 29 103 114 754.5 604~0 89' 7 110 1277 1216 29 103 1063 54 86

Source'

Alouatta

seniculus

pigra

palliata

fusca

caraya

belzebul

SP.

ma~connelli~~ straminea4'j

subsp.

palliata

equatorialis

7,170-8.000 7,000

3,560

6,500-8,150 7,620

7,880

11,113 11,590 8,060 9,000 6,200-7,300 5,400-8,172

7,938 6,917-7,825

4,770-10,910

5,200 8,400 7,400 7,670 6,900-8,700 5,600-8,626 5,000-7,000 4,500-9,800 7,040-8,760 6,600-8,800

fusca

subsp.

5,300-7,150

4,500-9,250

5,000-7,300 8,280

6,000-8,300

4,000-9,600

7,180 6,540-8,000

7,000

subsp.

subsp.

(?)

(28)

(4)

(1) (1) (14) (10) (3)

(1)

(1)

(60) (2) (7)

(?) (12) (?) (?)

(1) (2) (15) (10)

(1) (1)

(4) (3)

(4)

(10) (3)

(2

(8)

(19)

6,577 6,290 6,350-6,530 5,200 4,250-4,650 4,300-7,000 5,500 4,200-6,500 6,020

6,577 5,670

4,550-9,090

5,400-7,300 6,350 5,925 5,900-7,300 4,600-6,600 4,000-6,OOO 3,100-7,600 5,800-6,800 5,500-6,600

4,100-5,000

5,600-5,800

4,600-5,400 5,410

3,800-5,200

5,180 4,850-6,200

6,000

5,000-8,000 6,000-10,000 7.400

4,000-8,800 3,119

6,174

5,500

6,750-7,250

4,273

4,712

5,372

7,000

rtinued)

110 58

1054 604110 8g8 7 1277 1216

21

833 3848 313 27" 35 21 57'6 43

42 11447

1054 103 108 844 112 113 1223 1054

10;12,21

604,'o

101j4

934 29 7 1054 103 98 123

Brachyteles

Ateles

SP.

Lago thrix

robustus subsp.

subsp.

fusciceps

geoffroyi

paniscus

arachnoides

marginatus subsp.

chamek paniscus

subsp.

lugens poeppigii

cana lagotricha

subsp.

Subspecies

SP. belzebuth

flaoicauda lagotricha

Species

Genus

8,300 13.800-15,000 9,250-10,200

6,500-9,200 9,000-9,200 5,470-6,887

7,400

8,410-8,640 5,200 6,000-8,000 8,166 9,450

7,730-9,550 8,890 7,750-9,000 7,420 7,450 7,787

7,264-9,800 8,450

3.600-5,000

6,100

8,000-10,000

5,800

12,000 6,900-9,300 9,500

9,000-11,000

6,500-8,500 8,500

10,000 7,031 8,590

6,590-10,000

7,491- 10,400 7,740 5,824 8,200-9,400 6,590-8,640 9,163 6,000-7,250 8,000 7,637 8,912

6,000

5,900

5,000-6,500

5,400 6,400

3,500

5,600-6,500

Female weights

5,540 5,260

(n)

6,670

Male weights

TABLE 1. New World monkey body weights' (continued) (4

7,000

5,400-9,000

6,500

4,000-4,190

8,000-10,000

Sex unknown weights 5,000-10,000 6,500 10,000

(2

(?)

(?) (2)

(?)

(9

(?)

(n)

69 555'

82 865 89* 55 58 86

8''

8l' 1216 88 7 127'

35

7 55 64435 35 21 32 112 113 21 313 604,10 27"

1054

35 67 35 35 85 35 35 35 29

812

Source' 9g4 29 1024.50 7 21 1216

(continued)

‘Taxonomy follows Mittenneier et al. (1988a). Weights are given in grams. All weights are on adult animals; data in bold face are on wild-caught specimens, others are on captive, or presumed captive, specimens (including seminatural environments and provisioned animals). Data on preserved specimens, or specimens that were noted as being abnormal (e.g., missing body parts), are not included, nor are data on pregnant females (when noted in the original source). Values or range are given, followed by sample size in parentheses. (?)indicates sample size was not provided by original source. ‘Sources are listedin Table 2. Sources which clearly drew their information from others (i.e., obviously secondary sources) arenot included. Exceptions are: sources noted by footnotes 19,23, 38,42,44, and 50; somesources which may repeat data for Pithecia and Chiropotes; and Schultz,whose 1941data may includesome of the same individuals reported in 1940. For Schultz and the pitheciine sources, data are not clearly attributedto another source and the reportedmean weights and/or sample sizes may be slightly different. Therefore, we chose to report all relevant sources here. 3Author(s) actuallygivesmeanvaluesplusstandarddeviationorstandarderrorofthemean. Herethes.d.01 s.e. hasbeenaddedtoandsubtractedfromthemean togiveaminimum range; the actual weight range would have been larger. ‘We assume these data are on wild-caught individuals, although the author does not specifically indicate that this is the case. 5The reference for some or all of these weights indicates the original source was a personal communication, presented paper, or other unpublished source. ‘Terborgh’s (1983) weights are taken from his Table 3.3 and text, pp. 30-38. Different values and averages given elsewhere in his text are not included here. ‘Wright’s (1985)data are taken in part from Janson(l975, which in turn were from other sources) and Terborgh (1983), but it is not clear which data are original. Therefore all of her data are repoked here along with those ofTerborgh (1983). 8A copy of the catalog for the collection housed in the Departamento de Zoologia, Museu Paraense “Emilio Goeldi” was most generously supplied by Dr. Jose de Sousa e Silva, Jr. Although most snecimens are likely adults. the catalog gives no indication of maturity of the animals. These data are a n extremely important and previously unpublished addition to our often meager knowledge of body weights of wild caught pra&rhines.Therefore, we have decided to make a n exception to our practice of not making any judgements on a data source. We exclude weights which, in our judgment, strongly appear to be juveniles, falling well below the normal range of weights for that species or genus reported elsewhere (as summarized here). If the weight is somewhatlow butin our judgmentpossibly representinga matureanimal, wehaveincluded it. Werecognizethatthisintroducesthepossibility ofsomeerror(ineither direction) a t thelow end of the weight range, but felt this compromise was preferable to exclusion of these valuable data. ’John Robinson (personal communication) indicates that these weights from Robinson and Redford (1986) are of wild-caught individuals. “Jungers’(1985) dataarefromatablegiving bodyweightdataspecifictoameasuredskeletalsampleforhisstudyas wellasdatadrawnfrom theliteratureandothersources.On1ythosedata indicated as specific to his skeletal sample (i.e., original to his study) are given here. 1’ThesedatafromHershkovitz(1977)listsequentialdatesonwhich weightsforagroupofanimalsweretaken, and themeansoneachdatearegiven.Althoughitisnotspecified,itapearsthat these are sequential data on the same animals, as all are from the San Diego Zoo primate colony (unpublished reports). Therefore, the range of means (lowest and highest values) is recorded here. ”Bauchot and Stephan’s (1967) weights are for laboratory animals, and often these are the lowest weights for the species. We include their data but recognize that they may not be representative of the species. 130nlydata on normal adults are used; those on adult “wasters” are excluded. “Rylands (1989) takes his data from that tabulated by Hershkovitz (1977) for animals Hershkovitz assumed were C. penicillata X C. j . geoffroyi hybrids. “In order to maximize the specificity of the data given in three tables in Soini (1981), we have chosen to emphasize subspecific differences over sexual differences. Therefore, we exclude the datain hisTable4, whichgives ameanvalueforSaguinusfuscicollis(subspeciescombined), but dividedby sex. Wereport his valuesforcombined sex samplesofS. f. illigeriands. f. fuscicoLlis from his Table 3, and take divided sex data for S. f. nigrifrons from his Table 5. Therefore, there may be some slight differences in the values we report here and those given in other sources which use Soini’s (1981) data. “Only Hrdlicka’s (1925) data on wild specimens of Alouatta p a l h t a inconsans and Saguinus geoffroyi (his Saguinus oedipusgeoffroyi) from his Table 1are used; Hrdlicka indicated that other data are generally from captive and abnormal animals, and the weights are extremely low. ”Dawson (1976) and Dawson and Dukelow (1976) give similar, although not identical weight data, presumably from the same sample of animals. We have chosen to use data reported in Dawson and Dukelow since they give larger standard deviations for approximately the same sample size. “Only Eisenberg and Thorington’s (1973) weights in theirTable 2, from Barro Colorado,areincluded here. The authors indicate that the weights from their Table 1were “adjusted,” and we are unclear as to what this means; therefore, weights from their Table 1 are not used here. Weights in Table 2 are from captive animal records (Thorington, personal communication). IgGarber and Teaford (1986)provide data without sample sizes, citing Soini (1982)as the original source. Snowdon and Soini (1988)give the sample sizes we repeat here for these same data, but they give the original reference as Soini and Soini (19821, same title. As Soini (1982) was unavailable to us, we report the weights given in the secondary sources here. ‘%bspecies is unspecified in sources listed here, weights could be for S. oedipus oedipus or S. oedipus geoffroyi, which is now raised to separate species status (S. geoffroyi). “Bauchot and Stephan (1969) cite another source for this weight but fail to include a complete bibliographic reference. Animals are assumed to be captive, laboratory specimens. “These data list two sequential dates on which weights were taken on the same animals. The mean of the two weights is given here. %xtenegger (1973) cites Hampton et al. (1966) for this weight. However, we are unable to locate this weight in the Hampton et al. reference. “Mostreferencesdo notdiscriminate between thespecies of Leontopithecus; therefore, some ofthedatagiven for L. rosaliamayactually pertain to oneoftheother twospecies now recognized. =These data were identified a s belonging to species Leontopithecus rosalia, as distinct from the other species of Leontopithecus now recognized. 26CQ~~irniC0 male weight is the mean of highest and lowest normal weights reported for the same animal. ”Most sources on Saimiri males do not indicate whether the data is for “fatted” (breeding season) or “non-fatted” individuals. Exceptions are noted by footnotes 29, 31, or 35. %rile and Quiring (194O)reportweights of 193gand 903g for a taxon which we assume is Sairniri sp., but this is not clear (listed as “Squirrel (marmoset) Leontocebus geoffroyi (Pucheran)”). These data are not included on this table. ”Author(s) indicate that weights were taken on males during breeding season (“fatted males).

30Weibeet al. (1988) list means for weights of 10 animals taken on sequential dates. Only the highest and lowest means are reported here for the sample of 10. 3’Author(s) indicates male weights were taken outside of breeding season (“non-fatted” males). ”Most sources treat this genus as monotypic; although Mittermeier et al. (1988a)now recognize more than one species. Therefore, some of the data listed for this most widely recognized species may actually pertain to a different species. 33Plooget al. (1963) provide a series of weights over a 12-month period for each of their five adult Saimiri. The mean for the series of each animal was computed and used here. %Male data are taken from Beischer and Furry’s (1964) Table 2, female data from their Figure 2; this was done to preserve the largest ranges presented. =DuMond (1968) provides average weights for both “fatted” and “non-fatted” Saimiri males. In this case, the lower weight is that for “non-fatted” males and the higher weight is that of “fatted” males. 36Weassume the weight for the female given here is of a pregnant individual, since the weight reported is 50%larger than any other source for Saimiri females. We report it here but do not include it in Tables 3 and 6. 37Thisspecies name was published after Mittermeier et al. (1988a) and therefore is not present in their taxonomic update. We recognize it here. 36Napierand Napier (1967) cite “personal communication from G. Hubbell” and Veterinary Officer’s Reports: Zoological Society of London, for these data. We have deleted all data from Napier and Napier (1967) which is clearly drawn from other sources, and checked and cited the original sources. 3 9 0 n Iweights ~ taken prior to shipment (“Departure” weights of groups A, B, C summed) were included here. 401tis unclear whether the weights reported in both Malaga, Weller, Montoya,Moro, and Buschbom (1991,wild data) and Malaga, Weller, Buschbom, and Ragan (1991, captive data) include some of the same animals. Since the sample sizes and weight ranges are different, and one set of weights was taken shortly after capture in Peru while the other was after 4-12 months in captivity in the US., both were included here. 4’Napier and Napier (1967)actuallyciteHershokovitz(1963)as providing this weight. However, no weightscould belocatedin Hershkovitz(l963).Wereport thesedata but donotinclude them in Tables 3 or 6, since the source is uncertain. 42Ayres(1986) indicates the original source for these data is Johns (1986-see Literature Cited). This was an unpublished report that was not available to us. 43 Hill (1960) gives this as Pithecia monachus capillamentosa; according to Hershkovitz (1987), Pithecia capillamentosa is a junior synonym for Pithecia pithecia pithecia. “Thesedata from Hershkovitz (1985)includeAyres’(l981) data. Weincludeboth Ayres’and Hershkovitz’datahere, since Hershkovitz’has alargersampleand slightlyexpandedrange, and provides no breakdown by individual specimens. Because of our manner of computing average body weights (see Table 3), this partial redundancy does not overweight Apes’ data. 45Weightswere taken a t initial estrus. ‘6Mittermeier et al. (1988a)do not recognize subspeciesof Cebus capucinus and Alouatta seniculus but indicate several may be valid. Therefore, to maintain the integrity of these data, the subspecies designations from the original source are retained. ::Scott et al. (1976) statethat they weighed some animals twice, but we are unable to determine which ones from the data. This only affects the sample size, which may be slightly inflated. This range is a range of means from different localities. No range of original weights, standard deviations, or sample sizes were given. 49 We assume Rudran’s (1979) data are primarily the same data reported as mean values in Thorington et al. (1979). Only the former is reported here for this species. “Robinson and Redford (1986) cite Leo (1984) for this weight. As Leo (1984) was unavailable to us, we report the weight given in Robinson and Redford (1986) as a secondary source. 51Numerousauthors give an estimate of 12,000-15,OOOg for Brachyteles, some citing Aguirre (1971) and some not citing anyone. Aguirre (1971) in turn cites Ruschi (1964) for giving the 12,000-15,000 range. For those not citing anyone, we have made the assumption that Ruschi (1964) in fact is the original sourceof all references giving a body weight of 12,000-15,OOOg and have not listed any of these other sources. 52Hill(1962) indicates these data are from Erikson (n.d. given). We assume data are on a captive individual.


433

TABLE 2. Sources used for body weight data‘ Source no.’ 1 2

3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62

Author/s (year) Ackerman (1991) Alexander SE, Yeoman RR, Williams LE, Aksel S, and Abee CR (1991) Altmann PL and Dittmer DS (1962, p. 350) Altmann-Schonberner D (1965) Aquino R and Encarnacion F (1986) Ayres JM (1981) Ayres J M (1986, Table 8.5) Bauchot R and Stephan H (1969) Beischer DE and Furry DE (1964) Benirschke K and Richart R (1963) Boinski S (1989) Bowden D,‘ Winter P, and Ploog D (1967) Buchanan-Smith (1991) Carmichael M and MacLean PD (1961) Christen A (1968) Cicmanec J L (1978) Coe CL, Smith ER, and Levine S (1985) Coimbra-Filho AF (1969) Coimbra-Filho AF and Mittermeier RA (1978) Cooper RW (1968) Crile G and Quiring DP (1940) Dawson GA and Dukelow WR (1976) Defler TR (1979) DuMond FV (1968) DuMond FV and Hutchinson TC (1967) Ehlers CL and Foote SL (1984) Eisenberg JF and Thorington RW Jr (1973) Elliott MA, Sehgal PK, and Chalifoux LV (1976) Emmons LH (1984) Epple G (1970) Estrada A and Coates-Estrada R (1985) Fedigan LM, Fedigan L, Chapman C, and Glander KE (1988) Flurer C and Zucker H (1985) Fontaine R (1981) Fooden J (1963) Fooden J (1964) Freese CH, Heltne PG, Castro RN, and Whitesides G (1982) Froelich JW and Thorington RW J r (1982) Garber Paul (personal communication) Garber PA, Encarnacion F, Moya L, and Pruetz J D (in press) Garber PA and Teaford MF (1986) Glander KE (1980) Glander KE (1987) Goldizen AW (1986) Grand TI (1977) Hershkovitz P (1977) Hershkovitz P (1982) Hershkovitz P (1983) Hershkovitz P (1984) Hershkovitz P (1985) Hershkovitz P (1987) Hershkovitz P (1990) Hill WCO (1957) Hill WCO (1960) Hill WCO (1962) Hoaee RJ (1978) Hrdicka A (1925) Husson AM (1978) Johns AD and Skorupa J P (1987) Jungers WL (1985) Kholkute SD (1984) Kinzey WG (1981)

Source no.’ 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114

Authoris (year) Kirkwood J K (1983) Kleiman DG (1976 Kleiman DG (1981) Klein R, Bleiholder B, Jung A, and Erkert HG (1985) Leutenegger W (1973) Lewis DH, Stein FJ, Sis RF, and McMurray DN (1987) Limos de Sa RM and Glander KE (in press) Lindsay NBD (1979) Lorenz R (1969) Lorenz R and Heinemann H (1967) Lucas NS, Hume EM, and Smith HH (1927) Lucas NS, Hume EM, and Smith HH (1937) Lucas PW, Corlett RT, and Luke DA (1986) Lunn SF (1983) Malaga CA, Weller RE, Buschbom RL, and Ragan HA (1991) Malaga CA, Weller RE, Montoya E, Moro J, and Buschbom RL (1991) McNees DW, Lewis RW, Ponzio BJ, Stein FJ, and Sis RF (1983) McNees DW, Lewis RW, Ponzio BJ, Stein FJ, Sis RF, and Levy BM (1983) Mendoza SP, Lowe EL, Davidson JM, and Levine S (1978) Middleton CC and Rosa1 J (1972) Milton K (1982) Milton K (1984) Milton K and Nessimian J L (1984) Mittermeier RA (1977) Mittermeier RA, Konstant WR, Ginsberg H, van Roosmalen MGM, and Cordeiro da Silva E J r (1983) Murie A (1935) Museu Paraense “Emilio Goeldi,” Departamento de Zoologia, Dr. Jose de Sousa e Silva, Jr, curator (personal communication) Muskin A (1984) Napier J and Napier P (1967) Nelson TW (1975) Neville MK, Glander KE, Braza F, and Rylands AB (1988) Neyman P F (1978) Oliveira JMS. Lima MG. Bonvincino C. Avres JM, and Fleagle J G (1985) Ploog DW, Blitz J , and Ploog F (1963) Pook AG and Pook G (1982) Pope BL (1966) Ramirez M (1988) Robinson J G and Janson CH (1986) Robinson J G and Ramirez CJ (1982) Robinson JG and Redford KH (1986) Rosenberger AL (1992) Rosenberger AL and Coimbra-Filho AF (1984) Rosenberger AL and Strier KB (1989) Rosner JM, Schinini A, Rovira T, Merlo R, Bestard R,and Maldanado M (1986) Rudran R (1979) Ruschi A (1964) Rylands AB (1989) Sanderson IT (1949) Schaller GB (1983) Schultz AH (19401 schuiti AH (mij Scott NJ Jr, Scott AF, and Malmgren LA I

~-~.

( 1 9%) _,

.


434

TABLE2 Sources used for body weight data’ (continued) Source no.’ 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129

Authorls (year) Snowdon PT and Soini P (1988) Soini P (1981) Soini P (1988) Stahl WR and Gummerson J Y (1967) Stevenson MF and Rylands AB (1988) Tardif SD, Clapp NK, Henke MA, Carson RL, and Knapka JJ (1988) Terborgh J (1983) Thorington RW Jr, Rudran R, and Mack D (1979) Thorineton RW Jr. Ruiz JC. and Eisenberg JF (1984) Weibe RH, Williams LE, Abee CR. Yeoman RR. and Diamond E J (1988) . ~. White F (1986) Wilen R and Naftolin F (1978) Wright PC (1985) Yoneda M (1981) Zieeler TE and Stott GG (1986)

‘See Literature Cited for full hibliographic references. ‘Refers to “Source” column in Table 1.

smaller estimate (around the size of Leontopithecus, or 596 g). Rosenberger et al. suggest Branisella may represent the ancestral size by virtue of the antiquity of this taxon, but it is not certain that this still poorly known monkey, from a locality that now appears to have been semi-arid to arid (MacFadden, 1990), is actually ancestral to all later New World monkeys. The slightly younger fossils from Argentina range widely in size (Fleagle, 1988, 1990). If the assumption that the body size of the earliest New World monkey is similar to that ofAotus and Callicebus is close to accurate (within a range of, say, 800 to 1,200 g), it can be used as a baseline to examine the directions and rough magnitudes of changes in body size in the various New World monkey lineages. It is this assumption that is followed here. Changes in body size that would result given the different taxonomic views are illustrated in Figures 5-8. Aotus and Callicebus themselves, as the two extant monkeys falling directly within this size range, have remained unchanged in body size regardless of which systematic arrangement is preferred. Therefore, changes in diet and feeding strategies in Aotus and Callicebus from any presumed ancestor and/or from each other must be explained in some manner other than simple body size

alteration or differences. These two monkeys are considered by finzey (1992). Again, regardless of systematic arrangement, the marmosets and tamarins have departed from the ancestral type by decreasing in body size to varying degrees. Leontopithecus (at 596 g) and Saguinus (at 464 g) have reduced body size approximately 50%,as has Callimico (492 g). Callithrix has reduced by about two-thirds (to 336 g). The smallest, Cebuella, has reduced body size by almost a complete order of magnitude, to slightly more than 100 g (123 g). At least some data suggest that Leontopithecus may have secondarily increased slightly in body size (Ford and Corruccini, 1985; Garber, 19921, as indicated in Figure 7. These phyletic dwarfs are discussed by Garber (1992). In all systematic arrangements, the sakiuakaris and atelines must have increased in size, from slightly to greatly. Following Ford’s view, slight increase to the size of Pithecia (about 1,000 to 3,000 g, with a mean of 2,094 g) would have occurred in the common ancestor of this group. Further increases would have occurred independently in the saki-uakari lineage, to around 2,000 to 4,000 g, and in the ateline lineage, increasing well over an order of magnitude to a mean of 10,788 g in Brachyteles. In the “classic”systematic arrangement (of Hershkovitz and others) and those of Rosenberger and Kay, any increases in body size from the ancestral body size would be independent in the saki-uakari and ateline lineages. These two groups are discussed by Kinzey (1992) and Strier (19921, respectively. Cebus and Saimiri are in some ways the most enigmatic. Their potential relationships to each other and to other New World monkeys remain unclear. However, in any scheme, if the AotuslCallicebus body size is considered ancestral, Saimiri has undergone some very slight body size reduction, to 836 g. This reduction would be independent of that found in the marmosets and tamarins in the taxonomic schemes of Ford, Dunlap et al., or the “c1assic”view.In Rosenberger’s arrangement, the decrease could have occurred only once, early in his Saimiril Cebuslmarmoset-tamarin group. However, if he is correct in his conclusion that Dolichocebus (with an estimated body weight of


435

TABLE 3. Mean body weights' Genus

Species

Cebuella Cebuetla

pygmaea

Callithrix Callithrix

argentata aurita emiliae flaviceps geoffroyi humeralifer jacchus kuhli penicillata SP.

Saguinue Saguinus

bicolor fuscicollis geoffroyi imperator la biatus leucopus midas mystax nigricollis oedipus SP.

Leontopithecus Leontopithecus

chrysomelas chrysopygus rosalia SP.

Callimico Callimico

goeldii

Origin

Male mean

Female mean

Unknown mean

M+F mean

Overall Mean

wild all wild all

130 145

126 128

113 113

128 136

123

130 145

126 128

113 113

128 136

123 128

wild all wild all wild all wild all wild all wild all wild all wild all wild all wild all wild all

286 286

261 284

371 374

274 285

336

357 357

320 320

338 338

338 338 429 429 320 320 406 406 273 273 323 323 257 307

429 429 310 310

330 330

320 320 406 406 340 340 380 380 279 297

290 290 280 280 256 255

190 190 310 310 236 371

225 225

182 182

wild all wild all wild all wild all wild all wild all wild all wild all wild all wild all wild all wild all

482 488

468 462

430 430 387 387 546 546

430 430 403 403 544 544

451 451

465 465

586 586 577 577 470 466 411 461

432 432 560 560 480 482 430 377

wild all wild all wild all wild all wild all

580 576

556 563

620 620 615 615

535 535

607 505 460

578 578 578

wild all wild all

278 502

500 483

278 502

500 483

240 240 295 295 246 313

128

345

375 340 340 425 425

204 204

454 477

476 475

464

330 343

430 430 395 395 545 545

430 430 373 377 545 605 450 450 497 497 440 440 523 498 542 542 435 436 420 436 445 445

725 450 450 575 575 440 440 552 477 489 489 355 360 472 445 445

700 700

700 700 700

458 458 509 509 568 568 415 474 420 419

375 249 249 425 425

469

568 569

596

578 578

578 578 615 615

592 541 519

628 594 579

600

389

492 389 492

(continued)

S.M. FORD A N D L.C. DAVIS

436

TABLE 3. Mean body weights' (continued)

Svecies

Genus Suimiri2 Saimiri

boliviensis oerstedi sciureus

ustus vanzolinii SP.

Aotus Aotus

azarae lemurinus nancymai trivirgatus SP.

Callicebus Callicebus

brunneus

cupreus donacophilis hoffmannsi moloch personatus torquatus SP.

Pithecia Pithecia

albicans irrorata monachus pithecia SP.

Chiropotes Chiropotes

albinasus satanas SP.

Ori~n wild all wild all wild all wild all wild all wild all wild all

Male mean

Female mean

911 956

703 702

1015 1265 829 829 852 829 910 910 950 950

700 800 695 695 675 569 795 795 650 650

Unknown mean 823 794

607 607 861 774

+

M F mean

Overall Mean

807 829

836

858 1033 762 762 764 699 853 853 800 800

858 1033 710 710 796 724 853 853 800 800 1000 1000

92 1 943

902

1000 1000

853

wild all wild all wild all wild all wild all wild all

932 941

910 945

955 955 923 961 920 925

780 780 968 968 940 888 950 840

923

1249

wild all wild all wild all wild all wild all wild all wild all wild all wild all

1048 1038

1049 1070

854 854 1012 1012 800 800

805 805 1119 1119


2384 2384

3000 3000 2010 2010 2795 2795 1732 1732

1875 1875 1900 1900 1515 1515

wild all wild all wild all wild all

3060 3060

2555 2555

2844 2844

2808 2808

2,862

3020 3020 3100 3100

2510 2510 2600 2600

2800 2800 2731 2731 3000 3000

2765 2765 2850 2850

2777 2777 2810 2810 3000 3000 (continued)

1000 935 1325 1325 1300 1300

920 920 860 983 1285 1285 1307 1307

93 1 978

1085 931 870

900 900

900 900

961 961 931 924 935 883

780 780 961 1003 931 924 934 878

1086

1086

1049 1054

1,005

830 830 1065 1065

830 830 1065 1065 800 800 920 920 920 939 1305 1305 1303 1303 900 900

930 959 1305 1305 1303 1303

900 900 1763 1763

1650 1650

1800 1800 1500 1500

934

2074 2074

1943 1943 2348 2348 2348 1623

1008

2,094 2094

3000 3000 1943 1943 2348 2348 1682 1682 1500 1500 2862


437

TABLE 3. Mean body weights' (continued) Genus

Species

Cacajao Cacajao

caluus melanocephalus SP.

Cebus Cebus

albifrons apella capucinus oliuaceous SP.

Alouatta Alouatta

belzebul caraya fusca palliata pigra seniculus SP.

Lagothrix Lagothrix

flauicauda lagotricha SP.

Ateles Ateles

belzebuth fusciceps geoffroyi paniscus SP.

Brachyteles Brachvteles

arachnoides

Male mean

Female mean

Unknown mean

M+F mean

Overall Mean


3450 3775 3450 3450

2810 3057 2880 2880 2740 2740

2975 2975

3130 3416 3165 3165

3,011

4100

3550

3825

3825


3093 3082 2480 2480 3050 3050 3868 4315 2974 2974

2315 2486 1814 1814 2385 2385 2666 3350 2395 2395

2704 2784 2147 2147 2718 2718 3267 3833 2684 2684

2,811

wild all wild all wild all wild all wild all wild all wild all wild all

7564 7512 7270 7270 6800 6800 6175 6175 7150 7705 11352 11352 7200 6280 7000 7000

5438 5572 5525 5525 4605 4800 4550 4550 5350 6095 6434 6434 5600 5600 6000 6000

5803 5803 5372 5372 4712 4712 4273 4273 5960 5960

6501 6542 6398 6398 5703 5800 5363 5363 6250 6900 8893 8893 6400 5940 6500 6500

6,415


8335 6800

5750 5000

7043 5900

8,398

8335 6800

5750 5000

8833 8167 10000 10000 9000 7000 7500 7500

wild all wild all wild all wild all wild all wild all wild all wild all

8273 7933 8532 8532 8890 8640 8210 7100 7460 7460

8280 8214 8112 8112 8800 7995 7456 8000 8750 8750

7048 6688

8276 8074 8322 8322 8845 8318 7833 7550 8105 8105

7,835

12125 12125 12125 12125

9450 9450 9450 9450

10788 10788 10788 10788

10,788

Origin

2975 2975

2838 2775 2500 2500 2500 2500 3101 2851 3250 3250

2593

7500 7500 7000 7000

7445 6365 7200 7200 6500 6500

7043 5900

3283 3165 3165 2858 2858

2804 2265 2265 2645 2645 3212 3505 2684 2684 3250 2921 6443 6056 6056 5372 5437 4999 4999 6153 6587 8893 8893 6767 6460 6667 6667 7922 10000 10000 7695 6267 7500 7500 7620 8322 8322 8845 8318 7704 7155 7803 7803 6500 6500 10788 10788 10788

'Mean values were determined as follows: Within species, the average of the lowest and highest values given in Table 1for each sex and sex unknown categories was determined. This approach was used to deemphasize any bias due to different (or unknown) sample sizes in different categories or from different authors. These one to three values were then averaged to derive the overall mean for species given here. We recognize that someindividuals prefer the average of male and female weights as a species mean, excluding sex unknown animals, so we report this mean as well. However, we choose to utilize the average of all three categories for an overall species or genericmean. since for some species, only weights for animals of one sex or all with sex unknown are available Wild-onlyand combined data were computed separately. The generic means (given in bold-face)are an average of the values for all species on which there are data. The overall mean value for wild-only data (underscored) is used as the generic mean in the text, except for Cullimico (where,the wild-only mean is based in large part on a single very small individual). Saimrrr male data included both fatted and unfatted males (see Table 1).

438

S.M. FORD AND L.C. DAVIS 4

“G+

Fig. 5. Directions of changes in body size, given the “classic” systematic arrangement of New World monkeys

2,700 g, Fleagle, 1988) is closely related to Saimiri, then decrease could have occurred at least twice following his view as well. An alternative interpretation of body size changes in this view would be one “trajectory” of size decrease, but with at least two reversals to size increase, in Dolichocebus and Cebus. Kay’s recent suggestion that Saimiri and the marmosets and tamarins are closely related to the exclusion of Cebus could also allow for a single event of size reduction to a squirrel monkey-sized animal. However, even in this view, independent size reductions in the Saimiri lineage vs. the marmoset-tamarin lineageb) is suggested by various fossils. In the Saimiri lineage, the existence of the slightly larger yet closely related fossil Neosaimiri (Stirton, 1951), the possibly related and similarly sized Lauentiana (Rosenberger et al., 19911,

and a new specimen from La Venta, Colombia (Kay, 19891,which is much smaller than Saimiri but retains a third molar (unlike the marmosets and tamarins), strongly suggests the patterns of size change in the Saimiri group (fossil and extant) are complex and unrelated to the history of size change in the marmosets and tamarins. A new, large (approximately 1,700 g) fossil from La Venta which exhibits a number of callitrichid-like dental features (Kay, 1990b) reinforces this view of independent events of body size decrease. Even among extant Saimiri, the average weight of males of three species falls well within the “ancestral” range (at 910 to 1,015 g). Regardless of which systematic arrangement is favored, Cebus has nearly tripled in body size (to 1,300 to 4,000 g, with a mean of 2,811 g) independent of all other New World monkey


439

A5

Fig. 6.Directions of changes in body size, given Rosenberger’s (1981)systematic arrangement of New World monkeys.

tors of clades tend to be small in body size, because relatively small taxa are often more generalized in form and adaptive strategies. But the real key to understanding size COPE’S LAW.. .OR STANLEY’S RULE? change is Gould’s (1988) observation that No discussion of size change through time the fundamental driver of change is an “inwould be complete without some consider- crease in the envelope of variation-the ocation of ways in which projected trajectories cupied size range” (pg. 323). For clades that conform with o r contradict Cope’s Law. On conform to Stanley’s expectation that the the surface, suggestions of size d e c r e a s e founding member will be at or near one extreme of the available size spectrum, the not once but perhaps twice o r more-would seem a direct violation of Cope’s Law. How- small end, then it indeed follows that inever, following Stanley’s (1973) exciting re- creased variability will result in more and interpretation of Cope’s views, Gould (1988) more larger taxa while retaining some a t the suggests we should think not in terms of small end of the available size range, as inevitable size increase through time, but Gould elegantly discusses. Many primate instead in terms of “Stanley’sRule”: the per- clades appear to conform to this model (body ceived tendency toward increases in body weights throughout this discussion are from size is due to sorting from initial small sizes. Fleagle, 1988, except for extant New World Both Gould and Stanley argue that origina- monkeys). For example: 1) the adapid Canlineages which have increased in body size. These two monkeys are discussed by Janson and Boinski (1992).

440


Fig. 7. Directions of changes in body size, given Ford’s (1986)systematic arrangement of New World monkeys.

tius torresi, at approximately 1,100 g, is the earliest known and the smallest notharctine and one of the smallest adapids; 2) the early omomyid Teilhardina is one of the smallest, at 90 g; and 3) the early anthropoid Qatrania is smaller than all but a few marmosets and tamarins, at 300 g. Even among catarrhines, all of which are much larger than most other primates, it appears likely that early catarrhines (e.g., Propliopithecus fraasi at 1,700 g), early cercopithecoids(e.g., Victoriapithecus at 7,000 g), and early hominoids (e.g., the small apes Mzcropithecus clarki at 3,500 g and Dionysopithecus a t 3,500 g) were at or near the small end of the current and past size range. Evidence for the “body size envelope” or range for strepsirhines is less clear, since the fossil record for strepsirhines is notably poor, and there is little evidence of the diversity that may have existed in the distant

past. However, some striking constraints are apparent among recent strepsirhines. Those on the mainland of Africa and Asia are clearly constrained to a body size somewhere between 70 g (Galagoides demidouii) and 1,200 g (Otolemur crassicauclatus, Perodicticus potto, and the Miocene fossil Progalago dorae). It is only on the island of Madagascar that strepsirhines appear to have escaped these size restrictions on the upper end, looming as large as 10 kg among the extant fauna (Indri indri) and possibly as large as 200 kg among the subfossils (Archaeoindris fontoynonti). A pattern is obvious here, although whether this pattern is also the reason behind the size constraints is less clear. Where anthropoids and strepsirhines are in moreor-less direct competition (mainland Africa and Asia and possibly Europe in earlier times), there is almost no overlap in body


44 1

Fig. 8. Directions of changes in body size, given Kay’s (1990a) systematic arrangement of New World monkeys

size distribution, along with various divergent ecological strategies, as pointed out by Fleagle (1978). The two groups appear to compete t o a sufficient degree that each competitively and quite effectively excludes the other group from its size range. Others have suggested a shift among Miocene through Recent primates to larger body sizes than those characteristic of the majority of early Cenozoic primates (e.g., Covert, 1986; Fleagle, 1978, 1988); however, the small end of the size range is still well represented in extant strepsirhines and may have been a major part of the primate radiation throughout the Neogene in the still poorly known African fossil strepsirhine clade. This picture of size range diversity in the Old World strepsirhines and anthropoids accords well with “Stanley’s Rule.” Although the origins of the strepsirhine clade are still shrouded in some mystery, its members

have been tightly constrained in a size-envelope ranging from 70 to slightly more than 1,000g, except on Madagascar. There, a lack of both competitors and many predators has released whatever constraints exist on the mainland toward increases in body size; however, constraints at the small end have remained, allowing widening of the envelope of variation in only one direction. Until fairly recently, one could confidently claim that early anthropoids fell at or above the mainland strepsirhine upper limit, and at the low end of the range of Old World anthropoids (e.g., late Eocene Pondaungia a t 7,000 g and Amphipithecus at 8,600 g; Oligocene Oligopithecus at 1,500 g, Apidium ranging from 850 to 1,600 g, Parapithecus fraasi at 1,700 g, and Propliopithecus ranging from 4,000 to 5,700 g). Extant catarrhines range from 1,250 g (the talapoin monkey) to 175,000 g (male gorillas), with fossil

442


forms which were even larger; no known catarrhines have ever been smaller than 1,200 g. Three fairly new fossils from the Fayum, all described as early anthropoids, would, however, extend the body size range of early anthropoids well back into the strepsirhine size range. These are the earliest Oligocene parapithecid Qatrania (300 g) and the late Eocene oligopithecines Catopithecus (from published photographs, the size of its first molars falls between those of Aotus and Saimiri, suggesting a body weight around 870 g) and Proteopithecus (from published photographs, its first molar is slightly smaller than that of Saguinus geoffroyi, suggesting a body weight around 500 g) (see Simons, 1989,1990; size estimates our own). Catopithecus, at least, was well within the range for the New World monkeys Aotus and Callicebus. Nonetheless, it appears likely that the earliest anthropoids were small by Old World anthropoid standards, and that although a small number of the earliest were very small, they quickly stabilized at a minimum size of around 1 kg. Competition with strepsirhines has likely precluded decreases in size in Old World anthropoids from this stabilized minimum. New World monkeys become the exception that proves the rule-Stanley’s Rule. The New World monkey fossil record, while growing rapidly, is still too sparse in the earliest time periods (see Fleagle and Rosenberger, 1990, and refs. therein) to allow the sort of histograms of size distribution through time that Stanley (1973)advocated. However, as presented above and in earlier work by SMF, a very strong case can be made that the ancestral New World monkey was around 1 kg in body size. This size is near the low extreme for extant catarrhines and probably near or at the low end of the “size envelope” for Old World anthropoids. Thus, prior to entry into South America, the early member(s) of a diverging New World monkey clade, at 1 kg, represented a fairly generalized anthropoid a t or near the small extreme of the available size spectrum for Old World anthropoids. However, once in South America and freed of competition with the smaller strepsirhines, it was a whole new ballgame. As “the envelope of variation” of body size in-

creased through time, it was free to do so in both directions. It is not surprising that multiple lineages (fossil and extant) appear to have explored each trajectory of change-to both increased and decreased body size. ECOLOGICAL IMPLICATIONS OF BODY SIZE CHANGE

A general relationship clearly exists between overall body size and numerous ecological/behavioral/physiologicaltraits for mammals in general (e.g., Alexander, 1977; Calder, 1984; Clutton-Brock and Harvey, 1983; Eisenberg, 1981, 1990; McNab, 1983; Peters, 1983; Schmidt-Nielson, 19841, leading Damuth and MacFadden (1990:2)to conclude that “a mammal’s body size may be the most useful single predictor of that species’ adaptations.” The inverse relationship between metabolic rate and body size is particularly strong and well-documented (Calder, 1984; Hildwein and Goffart, 1975; Kleiber, 1932, 1947; Lasiewski and Dawson, 1967). Other correlations vary in their strength, and many may actually be correlated with body size solely because of their relationship to metabolic rate (see, e.g., Eisenberg, 1981; McNab, 1980). As Clutton-Brock and Harvey (1983) comment, the effects of body size appear to be so great and to impact on so many features in complex and interactive ways, that identifying any narrow, specific relationships between body size and individual ecological factors is difficult. A very few of the size associations can be tied to absolute values of body mass as key indicators. Primary among these is the expectation that smaller animals will have higher protein content in their diets, associated with their higher basal metabolic rates and higher energy needs (Kleiber, 1947, 1961; also Clutton-Brock and Harvey, 1983; Eisenberg, 1981, 1990; Martin, 1990; Schmidt-Nielsen, 1984). Among primates, “Kay’s Threshold of 500 g is the direct expression of this relationship, where insectivorous primates tend to weigh less than and folivorous primates tend to weigh more than 500 g (see Fleagle, 1988; Martin, 1990; this is parameter I, Tables 4 and 5). Kay (1984) in fact stated that no primarily insectivorous primates would weigh more than 350 g (i.e., with more than 30%to 40% of their diet


composed of insects), and no primarily folivorous primate could weigh less than 700 g. The converse, that larger animals can afford t o have less protein in their diets and lower quality diets overall, generally appears to result in larger animals indeed having less protein in their diets. However, as CluttonBrock and Harvey (1983:651) caution, “that large species can feed on low quality food does not explain why they do so. One might expect both large and small species to feed on the highest quality food available to them” (see also Martin, 1990). As a second variable tied to absolute body size, Martin (1990) notes that small mammals, including primates, tend almost universally to be nocturnal, with a modal body weight for nocturnal primates at 500 g (this is parameter 111,Tables 4 and 5); only large mammals (especially those exceeding 5 kg) tend to be primarily diurnal, with a modal body weight for diurnal primates at 5 kg (he notes that marmosets and tamarins are one of the rare exceptions to this basic rule). Martin agrees with Charles-Dominique (1975) that this may be due to competition with diurnal birds, which are much more successful, limiting diurnality primarily to mammals larger than the upper limit for flight. Most posited size relationships, however, are more general: “Smaller” animals do “this,”“larger” animals are more likely to do “that.” Clutton-Brock and Harvey (1983) suggest most size-related features fit this mold, and that relative size within a taxonomic group, members of which share a basic mode of life, is a better predictor of ecological niche than is absolute body size. This is because the underlying adaptive mode of a group of organisms would often constrain its members from utilizing some types of resources, even should they become available (e.g., an ungulate is unlikely to become insectivorous, even if increasing numbers of slower moving insect prey become available, just as a bat is unlikely to become a grazer). Suggested general size relationships include the following: (1)(Parameter 11,Table 4)While metabolically, smaller mammals need higher protein levels in their diets and larger mammals can afford to exploit lower quality food

443

resources, as discussed above, aspects of general structure further differentiate the types of food niches animals of differing size may exploit. Larger animals can physically capture or handle larger prey, within carnivorous and insectivorous guilds, and utilize larger, tougher fruits and nuts, within frugivore/omnivore guilds (Clutton-Brock and Harvey, 1983; Peters, 19831, and they may do so to avoid competition with smaller species. (2) (Parameter IV,Table 4)Smaller mammals will tend to have a higher reproductive rate, with larger litters, rapid growth rates, and shorter maturation times, while larger mammals will produce fewer but often relatively larger neonates (Clutton-Brock and Harvey, 1983; Eisenberg, 1981; McNab, 1980). However, Clutton-Brock and Harvey point out that the evidence among mammals does not uniformly support these contentions. In fact, Blueweiss et al. (1978; see also Calder, 1984) found that relative neonatal weight scales inversely with adult body weight, with very small mammals’ having a neonate of roughly 10% of adult body weight. Leutenegger (1973) found the same inverse relationship for primates. (3)(Parameter V, Table 4)Larger animals will tend t o have increased longevity, due to their lower metabolic rates. In accordance with this, regular periods of torpor or hibernation may increase the life span of smaller animals with normally higher metabolic rates (Eisenberg, 1981). (4)(Parameter VI, Table 4) Larger animals will tend to have reduced relative heat loss. As discussed by Clutton-Brock and Harvey (1983) and McNab (1983 and elsewhere), this relates directly to Bergmann’s Rule; however, the cause of the basic relationship between body size and latitude remains somewhat obscure-it is not certain that it is directly due the decreasing temperature, or increasing seasonality, with increasing latitude. Nonetheless, with increased body bulk relative to exposed surface area, large animals lacking greatly projecting appendages (limbs, tails, ears) should be at an advantage in colder climates and a disadvantage in warmer climates. Therefore, in hot climates such as the Neotropics, one might expect fewer large mam-


444

TABLE 4. Predicted ecological associations with changing body size in neotropical primates (see text) Parameter I. Diet, general

11. Diet, item characteristics 111. Circadian pattern IV. Reproductive rate V. Life span VI. Heat loss/ retention VII. Population density VIII. Home range IX. Day range/ resource distribution X. Displacement/ resource defense XI. Forest strata XII. Locomotion

Smaller size

smaller smaller/less erratically distributed resources, or rich patches easily displaced by larger spp./indefensible resources, unless rich advantage in lower strata, esp. if vertical cling more leaping unless relative branch size is small

Modal size (1 kg)’

Larger size

frugivorous/mixed, varies seasonally varied insects, varied fruits diurnal

fewer insects, more folivory (esp. above 6 kg) larger prey (if insectivorous) larger fruitdnuts diurnal, no nocturnal forms

singleton birth; 1 litter/ year; neonate 9.8’31 of maternal weight

may have litters at greater intervals; smaller or larger neonates?

12.6 years small ears, moderate limb and tail length

longer life span longer limbdears, other adaptations favoring heat loss (in tropics) lower density

-

more insectivorous/exudatvorous (esp. below 500 g) smaller prey, softer fruits, smaller nuts more nocturnal, esp. below 500 g may have larger litters; litters closer together; smaller or larger neonates? shorter life span if heat retention a problem, may get smaller/shorter appendages higher density

17-57/sq km, much higher where disturbed .5-20 h a .3-1.4 km/varied resources territorial, no mixed species troops/food somewhat defensible understory and lower canopy arboreal quadruped, some leaping, climbing

larger largerlmore erratically distributed resources can displace smaller spp./ clumped, more defensible resources will prefer upper canopy more climbing, suspension, long forelimbs if in canow

‘Based on Callicebus (see text and Table 5)

mals, and the larger animals that are present may have markedly elongated appendages a n d o r behavioral adaptations to deal with higher heat loads. The reverse would be true for small mammals in cooler, more temperate regimes. However, Eisenberg (1981) noted that heat loss is not as serious for small mammals if they can conserve energy by dropping body temperature occasionally (e.g., torpor or hibernation). (5) (Parameter VII, Table 4)Smaller animals will have higher population densities (Peters, 1983; Robinson and Redford, 1986). (6) (Parameter VIII, Table 4) Larger animals may exploit larger home ranges, in part due to morphological differences due to large size (longer limbs and longer strides), which allow them to travel longer distances with relatively less energy expenditure (Calder, 1984; Clutton-Brock and Harvey, 1977, 1983; Eisenberg, 1981, 1990; but see following paragraph). (7) (Parameter IX, Table 4) Larger mammals can exploit foods which are more widely or erratically distributed, again due to their ability to cover greater distances

with less energy expenditure. Indeed, Clutton-Brock and Harvey (1979) found that the large-bodied orangs and chimps both used ripe fruit (an erratically and widely dispersed food item) and had larger day ranges than did the smaller apes or forest-dwelling cercopithecoid monkeys. However, they did not find a close relationship overall within primates between day range length and body size. (8) (Parameter X, Table 4) In direct competition over feeding sites, larger animals can more readily displace smaller ones, due to sheer size. Thus, according to CluttonBrock and Harvey (1983:656), large size is advantageous if food resources are clumped and defensible (such as fruiting trees), but “small species are likely to be superior competitors’’ if food supplies are indefensible (such a s grasslands of finite size of mixed plant species or insects). This is not necessarily contradictory with the idea that larger species will tend to exploit larger home ranges; larger animals will be better able to travel between dispersed resource clumps. Eisenberg (1981) predicts that


small animals can only utilize widely dispersed resources if they can find and defend a very rich patch. The ability to survive nonproductive periods by torpor or food storage would further enable small mammals to use such resources, (9) (Parameter XI, Table 4) Large arboreal mammals will tend t o utilize higher strata in the forest. Among terrestrial species, locomotion is generally less costly in larger animals (Clutton-Brock and Harvey, 1983; Eisenberg, 1990; Schmidt-Nielsen, 1984). As Martin (1990) notes, in general, locomotion is closely linked to basal metabolic rate and energy, both in terms of energy availability and energy costs of locomotion. However, due to problems resisting the pull of gravity in a three-dimensional environment, it is less certain that locomotion is less costly for large arboreal mammals. Smaller mammals can more readily exploit fine terminal branches in an arboreal setting, due to their ability to easily move out onto thin twigs and bushes (Clutton-Brock and Harvey, 1977). This advantage, however, is only marked in the lower strata of the forest, where the few large branches intermixed with many small ones are primarily vertically oriented (tree trunks), which do not provide an easy and safe “seat” for a large mammal. In the canopy, large mammals (such as primates) can sit on the many large, more horizontal branches and pull twigs t o themselves to feed (Clutton-Brock, 1974). Fleagle and Mittermeier (1980) predicted a close relationship between choice of forest strata and method of locomotion, which in turn, they suggested was closely tied to body size (see below). As a result of these interrelationships, they suggested that large, suspensory primates would be found in the canopy, while small leapers would inhabit lower forest strata. (10) (Parameter XII, Table 4) Smaller arboreal animals will tend to do more leaping, larger ones to do more climbing or be more suspensory (Fleagle and Mittermeier, 1980; Fleagle, 1988). Martin (1990:487) suggests that, in part, the reduction in leaping in larger animals may serve to protect the bones, which may become “increasingly vulnerable to stresses and strains” with increasing body size (see Martin for thorough

445

discussion). Napier (1967) also noted that larger primates will tend to have increased prehensility for better stability. Both he and Cartmill and Milton (1977) noted that the key is not absolute body size but the ratio of branch size t o body size: as relative branch size decreases, the need for increased stability via grasping increases andlor spreading out over several supports in suspension increases. Large arboreal herbivores will need long forelimbs, both to travel over discontinuities in support by suspension and to reach food items far out on terminal branches (Cartmill and Milton, 1977). In the approach described herein, both absolute and relative size associations play a role. For adaptations supposedly tied to specific body sizes, hypotheses can be generated irrespective of phyletic trends in size increase or decrease. For more general or relative size-associated traits, a baseline for a clade becomes imperative for formulating hypotheses as to expected adaptations. For example, if an ancestor is a quadrupedal frugivore with a home range of 4 hectares, and the descendent is larger, the descendent could be predicted to: 1) develop a less high energy diet (e.g., become more folivorous);2) locomote more rapidly across space (e.g., a terrestrial animal will become more cursorial, an arboreal one will become more suspensory with more brachiation); and 3) exploit a significantly larger home range. Thus, while in the past, the ecological roles of New World monkeys have been examined using primarily a static, synchronic approach, we feel that we may enhance our understanding of these roles by exploring the relationship between ecological (including feeding) adaptations and evolutionary pathways to the attainment of current body size. In the case of New World monkeys and the hypothesized trajectories of size change described above, several hypotheses of adaptations can be formulated and tested. In addition to hypotheses based on absolute size correlations, adaptations associated with general size categories can be hypothesized by assuming an ancestor near the size of Aotus and Callicebus and possibly sharing their general morphologicallphysiologicall ecological features. One problem intervenes here, however. These more general hypothe-

diurnal

often large insects, nonflying insects

insects, verts., fruit, gum

Saguinus (7, 8, 20) 464 g

diurnal

nonmobile or slow prey

omnivorous

Leontopithecus (7, 8,14) 596 g

twins; 2 litters/ twins; 2 litters/ twins; 1-1.5 twins; 1 litter/ year; neoyear; neolitterdyear; year; neonate 12.9% nate 11.9% neonate 8.8% nate 9.6% of of maternal of maternal of maternal maternal weight weight weight weight

diurnal

gum, insects, verts., (fruit-1 species) often large insects, nonflying insects

Callithrix (7,8, 22) 336 g

quadrupedal, leaping (climbing)

quadrupedal, VCL

XII. Locomotion (in order of predominance)

quadrupedal, leaping (VCL)

variable, esp. low-mid

low

low

8-100 ha .47-2 km/ erratic resources

XI. Forest strata

5-28 ha .l-2.1 km/ erratic resources

not always dis- polyspecific placed/terrigroups often torial displaced/ territorial

.l-.5 ha .03-.1 km/rich patches

X. Displacement/ easily disresource placed/ defense territorial

VIII. Home range IX. Day range/ resource distribution

quadrupedal, climbing, leaping

mid

polyspecific groups/ territorial

36 ha 2 km/erratic resources

12 V. Life span 13 10 14 (years) ? large ears, long large ears, long large ears, long VI. Heat loss/ tails, sprawltails, sprawltails, sprawlretention ing/daily ing/daily (source' for ing/daily body temp. body temp. body temp. most data: 5) fluctuations fluctuations fluctuations 34-247/sq km 8-70/sq km VII. Population 2.3-78/sq km .05/sq km? density

111. Circadian pattern IV. Reproductive rate (source' for most data: 9)

diurnal

gum, insects

I. Diet, general

11. Diet, item characteristics

Cebuella (7, 8, 21) 123 g z

Genus (Sources)' Mean body weight

small soft fruit; large insects, rarely mobile prey diurnal

insects, fruit

-

Saimiri (1, 11, 18) 836 g

nocturnal

fruit, insects, leaves

Aotus (13, 19, 26) 902 g

diurnal

fruit, insects, leaves

Callicebus (12, 13, 19) 1,005 g

long tails, urine washing, sneezing, sprawling, resting/ 50-75/sq km

1.5-25/sq km

varied by species, low vs. mid quadrupedal, (leaping)

17-57/sq km (1 site with 400) .5-20 h a .3-1.4 km/ patchy & erratic resources neutral to avoidance/ territorial

/diurnal forag- resting/ ing at southern extreme of range

1.5-90/sq km (1 report of 150) 3.1-10 h a 17.5-250 h a 33-60 ha .25-.83 km/ .7-4.2 km/ 1 kmlerratic patchy & erratic & resources erratic patchy resources resources no overlap/ polyspecific polyspecific territorial? groups/ groups someterritorial? times displaced/not territorial mid, vaned vaned, dense low (near growth ground, vertical forests) rapid quadru- quadrupedal, quadrupedal (leaping) pedal, (leapand VCL ine and clikbing)

?

singleton; 1 singleton; 1 singleton; 1-2 singleton; about 1 litlitter/year; litterlyear; litters/year; ter/year; neonate neonate ? % neonate 9.9% neonate 10.8%of maof maternal of maternal 28.6% of maternal weight weight weight ternal weight 21 12.6 ? 9

diurnal

nonflying insects, large insects

Callimico (7, 8,10) 492 g

TABLE 5. Actual ecological parameters in neotropical primates

singleton; 1 litter/vear: neonate ? 6 of maternal weight

diurnal

fruit, seeds (leaves) soft and hard seeds

upper canopy

mid to low

insects, fruit, nuts large fruit, hard nuts; small, hidden, slow prey; larger verts. diurnal

Ceb us (6, 11, 18) 2,811 g

5-131/sq km (1 report 1,040) 3-125 h a .l-1.3 km/ evenly distributed

5-40/sq km

neutral/antagonistic but not temtonal upper canopy, all slow quadrupedal, climbing

sprawling, resting/

resting/

50-260 ha 1-3.6 km/ erratic & patchy resources displaceothers, displace incl. howlers smaller, can /not terribe displaced torial? Itemtorial? varzea, varied varied, esp. high quadrupedal, quadrupedal, leaping (leaping and (climbing) climbing)

? ?/ patchy resources

?

resting/

singleton; 1 litter/l-2 years; neonate 9% of maternal weight 13

diurnal

leaves, fruit

Alouatta (3, 15, 23) 6,415 g

quadrupedal, suspension and climbing

upper canopy

neutral/not territorial

400-740 ha? 1-3 km/patchy resources

5-35/sq km

singleton; 1 litterA.5-2 years; neonate 7.8% of maternal weight 12

diurnal

fruit

Lagothrix (17, 18, 23) 8,398 g

upper canopy

often displace others/not territorial

70-300 ha? .35-1.6 km/ patchy resources

2.5-17/sq km

resting/

?

singleton; 1 litter/? years; neonate ? % of maternal weight

diurnal

leaves, fruit

Brachyteles (16, 18, 23) 10,788 g

quadrupedal, suspension suspension and and climbclimbing, ing (leaping) leaping (auadrupkdal)

upper canopy

often displace otherdnot territorial

100-389 ha .5-5 km/ patchy resources

2.4-24/sq km

long hindlimbs?/

singleton; 1 litter/2-4 years; neonate 5.8% of maternal weight 20

diurnal

fruit

Ateles (18, 23, 24) 7,835 g

'Numbers in parenthesesindicates sources: 1. Baldwin and Baldwin (1981);2. Buchanan et al. (1981);3. Crockett and Eisenberg(l986);4. Fontaine (1981);5. Ford and Corruccini (1985);6. Freese and Oppenheimer(1981);7 . Garber (1992);8. Goldizen (1986);9. Harvey et al. (1986); 10. Heltne et al. (1981);11. Janson and Boinski (1992);12. Kinzey (1981);13. Kinzey (1992);14. Soini Kleimanetal.(1988);15.Nevilleetal.(1988);16.Nishimuraetal.(1988);17.Ramirez(1988);18.Robinson andJanson(l986);19.Robinsoneta1.(1986);20.SnowdonandSoini(1988);21. 1988);22. Stevenson and Rylands (1988);23. Strier (1992);24. van Roosmalen and Klein (1988);25. van Roosmalen et al. (1981);26. Wright (1981). 'Indicates mean body weight.

XII. Locomotion (in order of predominance)

quadrupedal, leaping and leaping and quadrupedal, climbing (climbing)

polyspecific groupslnot territorial

avoidance? /?

X. Displace-

7 - 4 8 . 5 1 ~km (1 report of 1OO) 200-350 ha 2.5-5 km/ patchy resources

/bushy tail

4-10 ha ?/ patchy resources

ment/ resource defense XI. Forest strata

diurnal

fruit, leaves, seeds

Cacajao (4, 13, 19) 3,011 g

singleton; 1 singleton; 1 singleton; 1 litter/? vears: litter/3 litter/l-2 years; neoyears; neoneonate ? olc of maternal nate ? % (renate 10.3% ported small) of maternal weight weight ? 40 15

diurnal

fruit, seeds (leaves) soft and hard seeds

Chiropotes (13, 19, 25) 2,862 g

TABLE 5. Actual ecological parameters in neotropical primates (continued)

VIII. Home range IX. Day range/ resource distribution

V. Life span 13.7 (years) VI. Heat loss/ /dense fur, retention bushy tail, (source1 for sleep coiled most data: 5) up VII. Population 2-30/sq km density

pattern IV. Reproductive rate (source' for most data: 9)

111. Circadian

11. Diet, item characteristics

I. Diet, general

Pithecia (2, 13, 19) 2,094 g

448


ses are to a degree (though most assuredly not entirely) dependent on the assumption that the ancestor was indeed considerably like these two extant species, not only in body size but other adaptations as well. There is almost no way to test this assumption at present. Confounding this assumption is the fact that, despite the strong correlation of absolute size to basal metabolic rate across mammals, among the few primates which strikingly depart from the norm is Aotus. Like lorises and sloths, Aotus has a lower metabolic rate than would be expected for a placental mammal of its body size (Martin, 1990). McNab (1980,1986) has shown that in some cases, specialized diets (either folivory or myrmecophagy-anteating) can explain depressed metabolic rates (see also Elgar and Harvey, 19871,but such an explanation is not easily applied to Aotus. In fact, as noted earlier, Aotus has a remarkably high energy diet (with nectar and insects predominating at some seasons) for an animal of its size, much less an animal with a lower than normal basal metabolic rate. In addition, Aotus is nocturnal, although larger than 500 g, while all its close relatives (all other anthropoids) are diurnal, and given the lack of a tapetum, its nocturnality is almost certainly derived (Hershkovitz, 1983). It may be most appropriate, therefore, to use Callicebus (as described in Kinzey, 1981, 1992; Robinson et al., 1986) as a baseline for predictions of general size-related ecological patterns in New World monkeys (the two genera actually share many aspects of their behavior and general ecological roles). Predictions generated specifically for Neotropical primates based on the documented and hypothesized size associations in mammals discussed above are given in Table 4. The information provided by the other contributors to this issue forms a rich source for a test of these predictions, when supplemented primarily by data presented in contributions in Coimbra-Filho and Mittermeier (19811, Mittermeier et al. (1988b), and Smuts et al. (1986). It must be remembered, however, as Grand (1977, 1990) has pointed out, it is the outliers and the exceptions to general predictive models that can in fact be the most interesting and informa-

tive in questions of evolution. Therefore, in using New World monkeys as a data base for testing the predictions in Table 4,the exceptions must not be glossed over. We do not attempt a thorough test of these hypotheses here, but rather a brief examination of the evidence which may suggest areas ripe for future investigation. What emerges is both a picture of remarkable conformity with predicted adaptations and some truly intriguing exceptions, as summarized in Table 5 and below. For those parameters that can be measured quantitatively (e.g., neonatal weight), mean values for each genus were regressed against body weight (both variables logarithmically transformed) to determine if there is any clear relationship to size. For population density, both mean and maximum reported densities were regressed to body weight (see Table 6). 1. Diet, general Most smaller New World monkeys do have higher proportions of insects andfor exudates in their diets than characterizes either Callicebus or Aotus. However, within the smaller monkeys, there is no clear relationship between degree of insectivory or exudativory and body size (see Garber, 1992). Indeed, Leontopithecus may eat fewer insects than the larger Aotus. And although among the smallest of New World monkeys, one species of Callithrix (C. humeralifer) is highly frugivorous (Garber, 1992; Stevenson and Rylands, 1988). Cebus includes a remarkably high proportion of insects and vertebrates in its diet for a mammal its size (Janson and Boinski, 1992). Although Janson and Boinski do show that, in many ways, the diet of Cebus species relative to one another and to the much smaller Saimiri conforms to body size/ diet expectations, Cebus does have a very high quality diet contrary to predictions. Clutton-Brock and Harvey (1983) suggested some large mammals may include a high protein content in their diets because something about their behavior or morphology allows greater access to high protein food supplies than sympatric smaller mammals enjoy. Cebus does in fact selectively prey upon certain types of insects that it may be better able to exploit than sympatric mar-


449

Saimiri eats small, soft berries and other fruit, while Cebus and other larger monkeys reat large fruits and many with tough exoYParameter’ r square slope intercept P carps. Within the genus Cebus, it is only the Neonate -0.148 0.51 0.26 3.378 0.108 largest species, C. apella, that utilizes hard weight (to palm nuts on a regular basis (Janson and maternal Boinski, 1992). Use of hard nuts and seeds Wt.2) -0.331 Litter weight 0.84 0.71 4.899 0.001 also increases with increasing body size (to maternal among the pitheciines (knzey, 1992). Cebus Wt.2) routinely preys on more and larger verte0.117 Lifespan 0.40 0.16 1.842 0.171 Population 0.06 0.004 -0.085 3.603 0.822 brates than do the smaller predators (pridensity marily the marmosets and tamarins and Max. popula- 0.04 0.002 -0.058 3.929 0.887 tion density Saimiri). 1.059 -4.006 0.002 0.73 0.54 Home range However, among the insect foragers, the Home range 0.734 -1.412 0.020 0.61 0.37 predicted relationship between body size (excluding Cebuella) and prey size does not hold true. Small mar0.367 -2.526 0.058 Day range 0.52 0.27 mosets and tamarins frequently go after 0.098 -0.379 Day range 0.495 0.21 0.04 large insects, as does Saimiri, while the (excluding Cebuella) much larger Cebus selectively pursues many ‘Parameters as discussed in text and Tables 4 and 5. small insects. For these Neotropical insect 20verall mean used for Callimico, as no female body weights are foragers, prey behavior and ease of capture available. appear to be stronger determinants of prey choice than size of prey. Thus, the smaller mosets and tamarins or Saimiri, due pre- monkeys generally target slow or non-flying cisely to its larger size or other features of its insects or those not actively in flight. While morphology or behavior (see below). How- leaping is an important component of locoever, this is a static, synchronic interpreta- motion for many of these smaller monkeys, tion of an ecological parameter-it may ex- it is not used to gain access to prey in the air. plain how Cebus is able to exploit a Cebus, on the other hand, goes after large nutritionally rich resource, but it does not colonies of small, social insects. Its large size explain why it evolved this unusual diet in may be advantageous in gaining access to combination with its body size. At least two these insects, which are often hidden and of the largest New World monkeys do in- require considerable manipulation of the enclude a high proportion of leaves in their vironment to flush them out (see Janson diet, as predicted (Alouatta and Brachyte- and Boinski, 1992). Zes). However, as Strier (1992) discusses, it 111. Circadian pattern is contrary to body sizeldiet expectations Here, as noted earlier, the New World that Alouatta, as one of the smallest of the ateline group, is the most folivorous, and the monkeys form a marked contrast to the pretwo Neotropical folivores exhibit consider- dicted pattern in mammals. The smallest, able differences in their adaptations to a including many species below 500 g in body diet largely composed of leaves. As she weight, are uniformly diurnal, while Aotus notes, the slower locomotion characteristic is nocturnal at the relatively large size of ofdlouatta, in contrast to the faster activity 902 g. As reviewed above, many workers of the three largest atelines, is consistent have pointed out that taxonomic group (and with its unexpected (from a size perspective) by inference, evolutionary history) may be a more significant determinant of ecological lower energy intake. role than body size. In this case, the marmoII. Diet, item characteristics sets and tamarins, although absolutely Some aspects of primate dietary items do small by mammalian standards, belong to a conform to predictions. None of the smaller lineage (the anthropoids) that are historiNew World monkeys attempt to eat the hard cally diurnal and possibly, by design, almost nuts and seeds that some of the larger do. obligate diurnal mammals. Something very TABLE 6. Logarithmic regressions of parameters o n bodv weieht

450


unique must have acted (and continue to act) on the Aotus lineage, providing the impetus to derive away from this pattern and to return to a nocturnal activity rhythm, despite the lack of a tapetum (which is a significant structure for most nocturnal mammals). In addition, a very different competitive interaction may exist between neotropical birds and primates than between those in the paleotropics, allowing relatively tiny diurnal callitrichids to “violate” Charles-Dominique’s(1975)posited evolutionary determinant of mammalian activity pattern (see also Martin, 1990, and above). This may be an interesting area for future research. IV. Reproductive rate There is not a great deal of good life history data on many New World monkeys. However, true to prediction, the smaller New World monkeys have larger litters (twins). The exception here is Callimico which, although smaller than Leontopithecus, continues to have singleton births. Most marmoset and many tamarin litters are more closely spaced than those of Callicebus, producing up to two litters per year. It is worth noting that while Cullimico has smaller litters than the larger Leontopithecus, data suggest that Cullimico may reproduce twice as often (Masataka, 1981, but not according to Pook and Pook, 1981) or may have two reproductively active females in a single group (Masataka, 1981; Pook and Pook, 1981). This would effectively match the overall reproductive output of a Leontopithecus group, if not of a single female. Since Callicebus already has singleton births, larger New World monkeys could not further reduce litter size. However, evidence is strong that larger monkeys conform to predictions of greater investment in young by having offspring at longer intervals than every year, with midsized monkeys having interbirth intervals of 1 to 2 years and the largest with intervals up to 4 or more years. As discussed above, the literature actually offers two contradictory hypotheses on relative neonatal size. Theoretical models suggest that larger monkeys will have relatively, as well as absolutely, larger

neonates, while studies of actual weights across mammals document an inverse relationship between neonatal and maternal body weight, suggesting that larger monkeys will have relatively smaller neonates. Although Leutenegger (1973) claimed this inverse relationship was also found within New World monkeys, comparison of published birth weight to average female body weight from our Table 3 shows that, in fact, this ratio is largely constant across New World monkeys (see Table 5). Most New World monkey neonates weigh between 8.8% and 10.8% of maternal weight, hovering around the 10%value suggested as characteristic of very small mammals by Blueweiss et al. (1978). There are only a few exceptions, which tend to skew an allometric regression in the direction of negative scaling because they involve the very smallest and largest monkeys (see Table 6). Cullithrix and Cebuellu have somewhat large neonates (11.9% and 12.9%, respectively), and Lugothrix and especially Ateles have much smaller neonates (7.8% and 5.8%, respectively). The most exceptional monkey, however, is clearly Suimiri, which produces neonates almost three times larger (relative to maternal weight, at 28.6%) than the “norm” for New World monkeys. Thus, New World monkeys clearly do NOT conform to predictions that smaller monkeys should have relatively smaller neonates, and on the whole they also do not conform to expectations of an inverse relationship. When neonatal weight is multiplied by litter size, however, it is apparent that all of the monkeys smaller than 1 kg (with the single and interesting exception of Cullimico) produce a total litter weight 2 to 3 times that of all larger New World monkeys. Unfortunately, there are no reliable data yet available on neonatal weight for Callicebus, any of the saki-uakaris, or the largest New World monkey, Brachyteles, which severely limits any further interpretation of this aspect of reproductive strategy. But a regression based on available data for litter weight indicates a strong correlation and a very marked negative scaling to maternal body weight (see Figure 91, in agreement with Leutenegger’s work.


y 3 . 6 L 3.4

= -.331x +

4.899,

451

R-squared: .707

--- .==0

.I

1 . 4 . 1 . , . , . , 4.5 5 5.5 6

.

,

.

,

.

,

7 7.5 In(x) of Maternal Wt. 6.5

.

,

8

,

,

8.5

,

,

J

9

9.5

Fig. 9. Regression of log Litter Weight to log Maternal Body Weight. Dashed lines show 95% confidence limits of regression equation. (See Tables 5 and 6 for data, text for discussion.)

V. Life span Most authors agree that data on life span in the wild are limited and probably greatly underestimate actual life span. The available data (given in Table 5) would suggest that, for the most part, life span is relatively constant across New World monkeys with a low correlation coefficient to body weight (see Table 6) and therefore does not conform to predictions of an increasing relationship with body size. The largest monkey for which there are data, Ateles, does have a somewhat longer reported life span than most other monkeys (at 20 years). However, this is matched by the much smaller Saimiri (21 years) and greatly exceeded by Cebus (40 years), which is about one-third the size of Ateles. The smallest New World monkeys do not have noticeably shorter life spans. VI. Heat losdretention Very little work has been done on adaptations for heat loss or retention in anthropoid primates, much of which is reviewed in Ford and Corruccini (1985). Expectations of morphological adaptations to temperature

stress, focusing on limb, tail, and ear length, are often confounded by the fact that limb and possibly tail length appear to be partly constrained by locomotor requirements (see, e.g., Fleagle, 1988; Jungers, 1985). Limb length in particular is almost always examined in relationship to locomotor mode and analyzed as inter- and intramembral indices, rather than with a focus on heat loss/ retention. As Ford and Corruccini (1985) discussed, there is evidence that marmosets and tamarins are subject to both cold and heat stress at different times. Larger New World monkeys likely suffer only from heat stress in the Neotropics, although it remains possible that some monkeys which range into high altitudes, such as Lagothrix, or high latitudes, such as Aotus, may suffer periodic cold stress also. No clear relationship between body size and limb length that could be explained as an adaptation €or thermoregulation is apparent. Data presented in Jungers (1985, his Table 2) show that the large Lagothrix does have very long forelimbs while the small Cebuella has remarkably short forelimbs; however, as he dis-

452


cusses, this is almost certainly due to adaptations related to locomotor needs. No pattern is as evident in the hindlimb, where Saimiri has a longer hindlimb than several both smaller and larger New World monkeys. Contrary to predictions, Ford and Corruccini found a clear allometric trend to both longer tails and larger ears with decreasing body size in New World monkeys, suggesting that the smaller monkeys have developed morphological adaptations to heat stress lacking in the larger ones. Exceptions to these general relationships are an unusually long tail in Cebus and unusually small ears in Saimiri. Marmosets and tamarins have apparently adapted physiologically to cold stress, showing marked fluctuations in daily body temperatures (see discussion in Ford and Corruccini), consistent with predictions by Eisenberg reviewed above, as well as huddling behaviors. It has been suggested that the dense fur, bushy tail, and tightly coiled sleeping posture of Pithecia may function to conserve heat (Buchanan et al., 19811, which may also be true of the dense pelage of Lagothrix. Most New World monkeys appear to deal with heat stress primarily by behavioral adaptations, which largely include long periods of resting, particularly in midday, and adoption of a sprawling position for rest, with the limbs and tails spread out to allow maximum surface radiation of body heat. This appears to be particularly true for the largest monkeys with the lowest quality diets, Alouatta and Brachyteles, which are reported to spend a major portion of each day resting in stretched out positions. Garber (personal communication) has noted that Saguinus mystax and S. fuscicollis are very conservative in the amount of time spent in active pursuits throughout the year, generally rising late in the morning, resting much of the day, and returning to a sleeping site early. Saimiri (with its unusually short ears) has been suggested to use urine washing and sneezing as behavioral mechanisms to dissipate heat (Rosenblum and Schwartz, 1982). Behavioral adaptations to cold stress are also apparent, ranging from huddling and sleeping in coiled positions, as discussed above, to a switch to more daytime foraging in Aotus in the southern (i.e., coldest) ex-

tremes of its range (Robinson et al., 1986; Wright, 1981). VII. Population density As can be seen in Table 5, broad ranges for population density have been published for all New World monkeys, with many reports indicating considerable intrageneric and even intraspecific variation. These ranges largely overlap across almost the entire body size range, contrary to predictions, resulting in an extremely low and insignificant correlation with body weight for both average and maximum reported densities (Table 6). The very smallest (Cebuella), which uses a rich and concentrated food resource, does show remarkably high population densities in some cases, and the largest (Ateles and Brachyteles) do show consistently low population densities despite differences in their diets. However, their low population density estimates are no lower than those for the much smaller Callimico or Leontopithecus, and Alouatta, although quite large bodied, exhibits strikingly large population densities (in marked contrast to Brachyteles despite their dietary similarities-see Strier, 1992). Therefore, New World monkeys clearly do not follow predictions for mammals in general. VIII. Home range

In contrast, home range size does strongly support the predicted relationship of smaller monkeys having smaller home ranges, even given marked variability for each genus (see Table 6, Figure 10). The very tiny home ranges of Cebuella pull this regression somewhat, but even excluding Cebuella, there is a strong correlation and marked positive slope. There are only a few notable exceptions to the general rule. Some Saguinus populations (these are most likely species-specific differences) have unusually large ranges, although still not approaching those of the largest New World monkeys, as do some Saimiri populations. Chiropotes also tends to have extremely large home ranges for a midsized monkey. And Alouatta populations appear to have remarkably small home ranges given their body size. While this last has often been explained by


y

4.5

5

5.5

=

1.059~

6

-

4.006,

453

R-squared: .537

6.5 7 7.5 In(x) of Weight

8

8.5

9

9.5

Fig. 10. Regression of log Home Range Size to log Body Weight. Dashed lines show 95% confidence limits of regression equation. (See Tables 5 and 6 for data, text for discussion.)

the easy availability of their leafy diet, the same is not true of Brachyteles (see Strier, 1992). IX. Day rangehesource distribution Day range, contrary to predictions, is fairly constant across the body size spectrum for New World monkeys, generally ranging between 0.25 and 2 km. There are only a few exceptions to this. The smallest New World monkey, Cebuella, has undoubtedly the smallest day range, usually restricting travel t o one tree. This tiny range results in a skewed, seemingly positive relationship with body weight (see Table 6). When Cebuella is removed, the correlation becomes insignificant and the regression slope essentially 0. Although Cebuella’s resource is somewhat patchy (exudates), it is extremely rich, with one tree sometimes providing ample foods for an entire Cebuella group (family) for much of the year. For the same reason, the abundance of their food resource, many Alouatta populations also show an extremely short day range. While the folivorous Brachyteles also has short day ranges, Strier (1992) notes that in competition with Alouatta, the larger Brachyteles

always exhibits longer day ranges. However, she relates this more to Brachyteles’ higher quality diet (which is contrary t o prediction, see above) than to body size. Some Saimiri and Ateles groups and, especially, Chiropotes have remarkably long day ranges, yet these monkeys differ markedly from one another in diet and many other ecological and behavioral attributes. Body size does not appear to provide a simple explanation for these long day ranges. Predictions suggest that larger monkeys should be able to exploit both more patchy and more erratically distributed resources. Clearly, larger monkeys utilize fruit, a highly patchy resource, t o a much greater extent than smaller monkeys. However, some Saguinus species and one Callithrk species have been reported as exploiting a highly frugivorous diet (Garber, 19921, and there is no clear trend to increasing reliance on patchy fruits across the 2 to Il-kg body size range. Although exudate trees may also be patchy in distribution, they are a very rich resource, allowing the tiny Cebuella t o exploit them effectively. Insects can be erratic in distribution, contrary to predictions that smaller monkeys would avoid errati-

454


cally distributed resources. However, insects are also sufficiently abundant in the Neotropics that their distribution does not appear to be a constraint for small monkeys. X. Displacementlresource defense Many midsized New World monkeys are described as having neutral relations with other species; that is, they neither displace them nor are displaced by them. Several routinely form polyspecific groups with animals of different body size, and often displacement of one or the other is not readily apparent. I n the cases where it does occur, the relationship with body size is generally upheld. However, reports indicate that Callithrix is not always displaced by larger species, and Alouatta individuals are often displaced by smaller Cacajao or Cebus individuals (Fontaine, 1981; Freese and Oppenheimer, 1981). Contrary to predictions, smaller monkeys are territorial. However, one of their primary resources, insects, is a more or less indefensible resource, as predicted. Although larger New World monkeys do often exploit clumped resources, such as fruiting trees, there is little evidence that these resources are defended. And the more folivor o w species, which are among the largest, are of course utilizing an indefensible and non-clumped resource. Therefore, New World monkeys largely contradict predicted patterns of resource defense. XI. Forest strata New World monkeys conform strikingly to predictions on forest strata preference. Larger New World monkeys clearly prefer the canopy and upper levels of the forest. The smaller monkeys tend to favor lower strata (even down to ground level in some cases), dense secondary growth, or vertical forests (e.g., the bamboo forest habitat of Callimico). Medium sized monkeys favor mid-range strata o r range widely through vertical levels in the forest. It is unclear whether this is merely a n artifact of separate correlations of locomotion and strata preference, and locomotion and body size (Fleagle and Mittermeier, 1980). However, as discussed below, the relationship between locomotion and body size

is not absolute. Another possibility, relating back to queries on the surprising diurnality of the small marmosets and tamarins, is a preference for low forest strata as a way of avoiding competition with and/or predation by birds. An interesting test would be a detailed examination of forest strata choice by Old World primates, where small taxa are almost invariably nocturnal.

XII. Locomotion Unlike almost all other predicted ecologicalhehavioral associations with body size, those for locomotor preference were themselves largely derived from studies of New World monkeys (Fleagle and Mittermeier, 1980; Fleagle, 1988). It would, therefore, be circular to test these predictions on the same taxa, which included Saguinus midas, Saimiri sciureus, Pithecia pithecia, Chiropotes satanas, Cebus apella, Alouatta seniculus, and Ateles paniscus. However, there are considerable data on other species which can be used to test these predictions. Most of the larger New World monkeys do engage in more suspensory and/or more climbing activities than do either Callicebus or Aotus. However, Pithecia, at more than twice the size of Callicebus, is predominantly a leaper of striking agility (Buchanan et al., 1981; Kinzey, 1992; Norconk, personal communication), and leaping has been reported a s fairly common in the otherwise suspensory, very large Brachyteles (Nishimura et al., 1988). Many of the smaller New World monkeys do leap to a significant degree. However, leaping does not always increase with decreasing size below 1 kg. Saimiri oerstedi is primarily quadrupedal (Boinski, 19891, as is Leontopithecus (Kleiman et al., 1988). And although in general Saguinus species are similar in their locomotor styles, there are significant percentage differences in the use of different modes during travel. Saguinus fuscicollis, one of the smallest species (mean weight of 373 g), leaps only 32.5% of the time but climbs/ grasps 12.4% of the time, while Saguinus geoffroyi, which is much larger (mean weight of 545 g), leaps 41.5% of the time and climbdgrasps only 7.4% of the time (Garber, 1991), contrary to predictions.


In sum, while some predicted ecological associations with body size are found in many New World monkeys, there are a significant number of exceptions. Of the twelve predicted associations, strongest agreement is found for choice of forest strata, and good agreement (with a few exceptions) for diet and home range size. Either no size related association or the reverse of th at predicted is found for circadian pattern, life span, population density, day range and resource distribution, and displacement and resource defense. The remaining four variables show a rather mixed degree of concordance with predictions. Body size and dietary item characteristics largely follow predictions for fruit and seed choice, but not for prey size among insect foragers. Reproductive strategies follow predicted patterns in litter size, interbirth intervals, and litter weight, but not necessarily for relative neonatal size (for either of two contradictory predictions which can be offered). The smallest monkeys exhibit expected physiological adaptations for heat retention, but neither morphological traits nor behavioral adaptations for heat loss or retention follow predicted sizerelated patterns. And finally, New World monkeys generally follow predicted relationships between locomotor modes and body size, but the predictions were largely generated from studies of members of this group (as were those for forest strata preference); therefore, the many striking exceptions are perhaps all the more compelling a s a test of the predictions. Whether or not the many exceptions prove or disprove “the rules,” either for New World monkeys or for mammals in general, may be a matter of interpretation, interpretation that is difficult to undertake without better data from the field on most of these primates. The regression analyses performed here, for example, are generally based on very little data or on means drawn from a huge reported range of values; they must be considered very crude tests. McNab (1990) cautions that across mammals, significant variations from size-related patterns of behavior and ecology occur, and that predictions of body size associations should be based on very similar animals (phylogenetically, morphologically, and ecologically).

455

Taken in its narrowest sense, this constraint would preclude almost any predictions of general trends or size associations, including most that currently fill the literature (see review above); this is almost certainly a n unrealistically and unproductively broad restriction. Perhaps a more useful caution is that offered by Grand (1990:45), who notes that researchers “tend(s) to see weight as a numerical value in itself, unmindful of the major components of weight.” If we gain a better understanding of the differing ways body weight is distributed in animals and the evolutionary and functional basis of their development, the many “exceptions” in New World monkeys to general predicted associations may ultimately make a great deal of sense. SEXUAL DIMORPHISM Patterns of sexual dimorphism in body weight in primates have been widely discussed in the recent literature, with New World monkeys figuring prominently in many studies of correlates of sexual dimorphism (e.g., Cheverud et al., 1985a,b; Kay et al., 1988; Leutenegger and Cheverud, 1982; Leutenegger and Kelly, 1977; Smith, 1980). Many of these studies claim that marmosets and tamarins as a group are monomorphic or even negatively dimorphic (with females larger than males), and some make the same claim for Ateles. Several studies examining the causes and behavioral implications of sexual dimorphism have focused on overall body size as a major determinant, i.e., larger primates are more sexually dimorphic (Leutenegger and Cheverud, 1982, 1985). If this is so, examining sexual dimorphism in body size is highly pertinent to the present discussion of body size changes in New World monkey evolution. Others have suggested that social organization plays a key role in determining the degree of sexual dimorphism (e.g., Brown, 1975; Harcourt et al., 1986; Kay et al., 1988). There are many general statements and assumptions in the literature on the presence, degree, and nature of body size dimorphism in New World monkeys. However, these studies have all used data that are both less complete and less carefully screened (as to source, health and maturity


456

TABLE 7. Body weight dimorphism'

Genus Cebuella Cebuella Callithrix Callithrix

Saguinus Saguinus

Leontopithecus' Leontopithecus

Callimico Callimico Saimiri Saimiri

Aotus Aotus

Callicebus Callicebus

Species

Dimorphism ratio

pwmaea

1.028 1.028

argentata aurita emiliae flaviceps geoffw{ humeralifer jacchus kuhli penicilla ta

1.095 1.114 ? 0.939 ? 1.526 0.903 1.085 ? 1.236 1.030 -~ 1.000 0.960 1.004 ? 0.970

Genus Pithecia Pithecia

Chiropotes Chirouotes Cacajao Cacajao

Dimorphism ratio

Species albicans irrorata monachus pithecia

1.352 ? 1.072 1.471 1.144

albinasus satanas

1.198 1.203 1.192 1.228 1.198 ?

caluus melanocephalus

~

bicolor fuscicollis geoffroyi imperator la biatus leucopus midas mystar nigricollis oedipus chrysomelas chrysopygus rosalia' goeldii

1.336

albifrons apella capucinus oliuaceous

1.367 1.279 1.451 1.242

belzebul caraya fusca palliata pigra seniculus

1.391 1.316 1.477 1.357 1.336 1.764 1.286

?

1.355 1.029 0.979 0.955

Alouatta Alouatta

1.103 1.159 7

1.050

Lagothrix Lagothrix

? ?

1.296

boliviensis oers tedi sciureus ustus uanzolirzii

Cebus Ceb us

1.450 1.192 1.262 1.145 1.462

Ateles Ateles

Brachyteles Brachyteles

1.450 P

flauicauda lagotricha

1.450

0.999

belzebuth fusciceps geoffroyi paniscus

1.052 1.010 1.101 0.853

arachnoides

1.283 1.283

1.025

azarae lemurinus nancymai trivirgatus

? 0.986 0.981 0.968

0.999

brunneus cupreus donacophilis hoffmannsi moloch personatus torquatus

1.061 0.904

? ? 1.163 1.031 0.995 ~

~

~~~~

'Dimorphism expressed as male body weightlfemale body weight, using average species and genus weights from Table 3, for wild-caught animals except as noted. Mean genus dimorphism ratios in bold-face. 'Used captive data for one or both sexes because of missing data (see Table 3).

of animals, etc.) than the body weight data presented in our Table 1and summarized in Table 3. Given the critical nature of this area of research, we briefly present and summarize the evidence of dimorphism in

body size apparent from the data given herein (see Table 7). These ratios of dimorphism are based on the mean values for each species and genus in Table 3 (both wildcaught and total samples); since they are


ratios of single values, no statistics (such as standard deviation) could be computed. The discussion here focuses on dimorphism ratios of wild-caught animals. As can be seen in Table 7, most New World monkey species appear to be positively sexually dimorphic (that is, the male is larger than the female), either weakly or strongly. The most strongly sexually dimorphic include: Lagothrix, Alouatta (particularly A. pigra; A. seniculus is somewhat less sexually dimorphic than the other species), Cebus (although C. apella and C. olivaceous are somewhat less sexually dimorphic), Pithecia monachus (but not other Pithecia spp.), Saguinus midas (but not other Saguinus spp.), and Callithrix geoffroyi. Very slight positive dimorphism is also characteristic of Brachyteles, Cacajuo, Chiropotes, Pithecia pithecia, Callicebus moloch, Saimiri, Leontopithecus chrysomelas, and Callithrix argentata and C. penicillata. No New World monkey, however, approaches the marked positive dimorphism found in many Old World anthropoids, where the male may approach or even exceed twice the size of the female. The literature has often suggested that several New World monkeys are negatively dimorphic, that is, with the female larger than the male. From Table 7, it is apparent that only Ateles paniscus actually falls in this category. Two others have marginally low values, although these could reasonably be interpreted as monomorphy: Callicebus cupreus and Callithrix humerulifer. The remaining species would appear to be largely monomorphic, including: Ateles (except A. paniscus), Pithecia irrorata, Callicebus (except C. moloch),Aotus, Leontopithecus rosalia, Saguinus (except S. midas), Callithrix erniliae and C. jacchus, and Cebuella, All species in many genera have previously been assumed to be sexually dimorphic or monomorphic based on data on one or more “representative” species. What becomes clear from the data presented here is that, in fact, there are many cases where other species in the same genus prove to exhibit a different pattern. Genera with wide differences between species in pattern of sexual dimorphism of body weight (i,e., posi-

45 7

tive or negative dimorphism vs. monomorphism) include Ateles, Pithecia, Callicebus, Leontopithecus, Saguinus, and Callithrix. For some other genera, there are almost no body weight data by sex for many species (e.g., Lagothrix, Cacajao, Callicebus, Aotus, and Callimico), making intrageneric comparisons difficult. Kay et al. (1988) examined sexual dimorphism in canine size, and they also found intrageneric species differences, sometimes mirrored in behavioral differences. Our body weight data concur with their dental data in finding high positive sexual dimorphism in Alouatta caraya. However, there are significant points of departure between the two data sets. Three differences are readily explained by their incomplete sample of species. 1)They found all Callithrix to be monomorphic in canine size, based on C.jacchus. In fact, for body weight, several other Callithrix species are positively dimorphic. 2) They found Saguinus to be monomorphic in canine size, based on S. oedipus. For body weight, most species are monomorphic, including S. oedipus; however, S . midas appears to be positively dimorphic. 3) They also found Ateles to be monomorphic in canine size. Body weight data also shows monomorphism for most Ateles species. However, they did not examine A. paniscus, and the body weight data show this species to be negatively dimorphic, with females larger than males. More intriguing are the species in which body weight data and dental data give contradictory results. These include: Cebuella pygmaea, which is negatively dimorphic dentally but monomorphic in body weight; Leontopithecus rosalia, which is positively dimorphic dentally but monomorphic in body weight; and Callicebus, which is positively dimorphic dentally, but all except C. moloch are monomorphic in body weight. In addition, Lagothrix lagotricha is apparently only slightly positively dimorphic dentally, but markedly so in body weight. In the case of Leontopithecus, one cannot rule out the possibility of “hidden” species differences due to the lumping of most specimens into one species, L. rosalia, in most collections and studies. Nonetheless, the contradictions are striking, and we would concur with Kay et al. (1988) that selection for (or against)

458


sexual dimorphism in these two traits must greater differences in dietary strategy, locomotion, and other ecological factors between be due to separate factors. A particularly interesting case is that of Cebus and the similar sized large sakiPithecia. Only one species of Pithecia is uakaris. It is apparent that their common monomorphic in body weight, P. irrorata. body size was attained separately, and they The others are all positively dimorphic, P. exhibit markedly different behavioral reperpithecia very slightly and P. monachus toires (see both Kinzey, 1992, and Janson markedly. P. pithecia is unique from the and Boinski, 1992).A detailed comparison of other species in being sexually dichromatic these two taxa, from the perspective of the (Ayres, 19861, the other species being mono- evolution of contrasting adaptations in linchromatic (as are most New World mon- eages which have increased body size in parkeys). Apparently, different species of sakis allel, could prove instructive. Other issues center around Saimiri: 1) have responded to selection for differences between the sexes in markedly different what are its phylogenetic affinities; 2) did ways (the cause of which is at this point the extant genus attain its somewhat reduced body size independently of the marunclear). One troubling aspect of this study is that, mosets and tamarins (as suggested here) or as more body weight sources were added to as the result of a single event of body size Table 1, the pattern of dimorphism/ reduction; and 3) given the now two or more monomorphism for some species changed, closely related fossils, one larger and one particularly for those species that are not much smaller than extant Saimiri, haw does strongly dimorphic (i.e., with dimorphism one interpret directions of change in body indices of less than 1.25). Many if not all size and possible foraging strategies in this studies of body weight dimorphism (or other lineage? Similarities and differences in the associations and correlations with body feeding adaptations and locomotion of weight) rely on a small number of sources for Saimiri and the smaller marmosets and body weight. As can be seen from Appendix tamarins are still only poorly understood A and the footnotes to Table 1, some of the (see Boinski, 1989; both Garber, 1992 and sources which are commonly used or form Janson and Boinski, 1992). the basis of heavily cited secondary sources Aotus and Callicebus have a number of actually give highly questionable body morphological and behavioral similarities to weight data or appear to have included juve- one another and a few similarities to the nile or unhealthy animals (e.g., Bauchot and saki-uakaris, particularly for Callicebus Stephan, 1969, and sources cited therein). (see Kinzey, 1992). Do these reflect converHowever, if the differences among species of gences developed two or three times, a many genera of New World monkeys are shared retention of aspects of the ancestral real (and not an artifact of incomplete and New World monkey adaptive zone, or a skewed samples of body weight data), then shared heritage of inhabiting a new adapcareful evaluation of possible differences in tive zone, and just what is that as yet poorly ecological and behavioral attributes of the defined new zone? Given the frequent sugvarious species is called for. This may lead to gestions that one of these two genera (Aotus serious reconsideration of some now wide- and Callicebus) is the least changed from spread assumptions on the relationships the earliest New World monkey, these isbetween sexual dimorphism and other sues are of central importance to understanding platyrrhine evolution. attributes. The interesting morphological differences IMPLICATIONS FOR FEEDING between the many marmosets and tamarins ADAPTATIONS: DIRECTIONS FOR THE have led to some differences in opinion on FUTURE relationships within the group. These small A number of intriguing issues remain to monkeys range widely in body size, from 120 be examined, some of which we suggest g to 600 + g, and differ markedly in morhere. One involves the similarities and even phology and behavior (see Ferrari and Lopes

CHANGES IN P L A m R H I N E BODY SIZE

Ferrari, 1989; Garber, 1992; Sussman and Kinzey, 1984). Sorting out the evolutionary history and patterns of size change in these dwarfed monkeys, and relating these to a clearer understanding of feeding behavior, remains a n important area for further work. The largest New World monkeys, the atelines including Alouatta, are the source of several intriguing problems regarding the relationship between body size and ecology. Some of these issues are addressed by Strier (19921, including why a similar dietary adaptation, folivory, shows up at the two opposite body-size extremes within the group (BruchyteZes and Alouatta). Others include: 1)how do these largest New World monkeys compare ecologically to similar-sized members of other primate groups, particularly the Old World anthropoids; and 2) why did no New World primates become largerwhy are there no chimpanzee- or gorillasized primates in the Neotropics (other than the recent migrants, humans)? Similar questions pertain to the fossil record and interpretations of adaptive roles in the past. Several new small specimens have been recovered from the Miocene beds at La Venta, Colombia, including Micodon (Setoguchi and Rosenberger, 1985) and a new, unnamed specimen (Kay, 1989). Are any of these related to the extant marmosets and tamarins or did they attain small body size independently? Did all the small extinct New World monkeys fill similar or slightly differing adaptive roles, and to which (if any) among the modern marmosets and tamarins were they most similar? Complicating this issue is the discovery of a fairly large fossil from Colombia, similar in size to the largest species of Callicebus (C.personatus), with numerous callitrichid features in its dentition (Kay, 1990b). Cebupzthecza, also from the La Venta beds, is closely related to the saki-uakaris. While exhibiting many striking similarities to other members of this group, especially dentally (Fleagle and Meldrum, 1988; Meldrum and Fleagle, 1988; Stirton and Savage, 1951), there are a number of intriguing differences (Davis, 1987, 1988; Ford, 1990). These raise questions about changes within the saki-uakari group, particularly over

459

whether Pithecia retains the ancestral sakiuakari feeding adaptations or has independently altered its behavioral patterns (see Ford, 1990). These are only a few of the issues in ecological adaptations of New World monkeys that may be fruitfully investigated from the historical, evolutionary perspective we have advocated here. As Eisenberg (1990:25) stated, the goal and value of a n evolutionary perspective is a n understanding of the “consequences of becoming large or remaining [or becoming] small” (our addition). ACKNOWLEDGMENTS Many individuals have assisted at various stages of this project. We wish to thank Drs. Paul Garber and Warren Kinzey for first suggesting this topic to SMF and inviting her to participate in the exciting symposium that initiated this series of papers. Major and unceasingly patient assistance was given in tracing references and obtaining interlibrary loans by Ms. Kathy Fahey and Ms. Kim Stout; without their assistance Table 1could never have been compiled. Dr. Lionel Bender, Dr. Jonathan Hill, Mr. Michael Simons, and especially Ms. Elke Geisler all assisted in translating sources. Several individuals were very gracious in assisting us to interpret and evaluate published body weights, including Drs. Marcio Ayres, Paul Garber, Charles Janson, John Robinson, Alfred Rosenberger, and Richard Thorington, Jr. Drs. Paul Garber, Jose Sousa e Silva, and Karen Strier all provided important, unpublished body weight data, for which we are particularly grateful. And this paper has benefited considerably from the discussions and comments of Drs. John Fleagle, Paul Garber, Steven Gaulin, and Warren Kinzey, Monte McCrossin, and two anonymous reviewers, all of whom we thank. Partial support was provided by a grant from the Office of Research Development and Administration, Southern Illinois University. LITERATURE CITED Ackerman D (1991) A reporter at large (golden monkeys). The New Yorker June 24: 3G54. Aguirre AC (1971) 0 mono Bruchyteles aruchnoides (E.

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APPENDIX A Sources not used in Table 1 (body weights) A number of sources provided original data that we chose to exclude from Table 1, even though the author(s) did not indicate the animals were juvenile, pathological, or preserved. We were very conservative in making the decision to exclude any particular data, especially as some questionable references have been frequently cited in the past (e.g., Warnke, 1908). However, some data were so clearly aberrant or otherwise questionable that we did exclude them. These are listed below, along with the reason for exclusion. Many sources listed here are used in Bauchot and Stephan (19691, which is a heavily cited source for primate body weights in the literature. Note that several common platyrrhine body weight references (e.g., Fleagle and Mittermeier, 1980; Janson, 1975; Kay, 1974; Smith, 1980; and almost all data from Napier and Napier, 1967) were not used because they are secondary sources. The original sources are included in Table 1. The following list does not include the many sources that clearly indicated that the data were on juvenile, pathological, or preservedJfrozen individuals (these data were also excluded from Table 1). For additional information on sources or partial

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sources that were not used, see footnotes in Table 1. Bronson RT (1981) Brain weight-body weight relationships in 12 species of nonhuman primates, Am. J. Phys. Anthropol. 56~77-81. The author states that some weights are from pathological animals, and the weights for Ateles are very small. Crisp E (1865) On the relative weight of the brain, and on the external form of this organ, in relation t o the intelligence of the animal. Br. Assoc. Adv. Sci. Rep. Ann. Mtg., pp. 84-85. The weights for Ateles and Cebus are extremely low, and a reported marmoset brain weight is only approximately 2 g lighter than its body weight, putting all of the data in question. (This reference is cited in Bauchot and Stephan, 1969.) Eisenberg JF (1989) Mammals of the Neotropics, The Northern Neotropics, Vol. 1. Chicago: University of Chicago Press. Eisenberg does not provide original sources for many of the species, but it clearly appears to be a secondary source. Eisenberg JF (1979) Habitat, economy, and society: Some correlations and hypotheses for the Neotropical primates. In IS Bernstein and EO Smith (eds.): Primate Ecology and Human Origins. New York: Gartland Press, pp. 215-262. The only body weight given which is not given elsewhere is his weight of 600 g for Saguinus leucopus. This appears to be estimated from data on other Saguinus spp., and no reference for this weight is given. Fleagle J G and Mittermeier RA (1980) Locomotor behavior, body size, and comparative ecology of seven Suriname monkeys. Am. J. Phys. Anthropol. 52~301314. This reference is a secondary source. Hrdlicka A (1905) Brain weights in vertebrates. Smithson. Misc. COIL48:89-112. The author indicates that platyrrhines in this study were either emaciated or of a “medium nutritional state” (pp. 91-92). (This reference is cited in Bauchot and Stephan, 1969.) Janson CH (1975) Ecology and population densities of primates in a Peruvian rainforest. Undergraduate thesis, Princeton University. This reference is a secondary source. Kay RF (1974) Mastication, molar tooth structure, and diet in primates. Ph.D. dissertation, Yale University. This reference is a secondary source. Kennard MA and Wilner MD (1941) Weights of brains and organs of 132 New and Old World monkeys. Endocrinology 28:977-984. Authors indicate that some monkeys were diseased, and we could not be certain of differentiating the data on the healthy ones. (This reference is cited in Bauchot and Stephan, 1969.) Kulhorn F (1954) Gefugegesetzliche untersuchungen an neuweltaffen (Cebus appella L. und Alouatta caraya Humboldt). Zeit. Saugetierkunde 20:13-38. Although these weights look normal, the author indicates that the stomach and intestinal contents were removed prior to weighing. We felt it safest to exclude these data. Lang CM (1968) The laboratory care and clinical management of Saimiri (squirrel monkey). In LA Rosenblum and RW Cooper (eds.): The Squirrel Monkey.

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New York: Academic Press, pp. 393-416. Age of animals is unknown or unclear. Long J O and Cooper RW (1968) Physical growth and dental eruption in captive-bred squirrel monkeys, Saimirz sciureus (Letica, Colombia). In LA Rosenblum and RW Cooper (eds.): The Squirrel Monkey. New York: Academic Press, pp. 193-205. All specimens are immature according to adulthood estimates of Dumond (1968). Mangold-Wirz K (1966) Cerebralisation und ontogenesemodus bei Eutherien. Acta Anat. 63:449-508. The reported weights are very small. (This reference is cited in Bauchot and Stephan, 1969.) Nowak RM (1991) Walker’s Mammals of the World (5th Edition), Vol. 1. Baltimore: Johns Hopkins University Press. No sources are listed, although this (and all previous editions) clearly is a secondary source. Portmann A (1948) Die cerebralen indices beim menschen. Revue Suisse de Zoologie 55(2):257-260. The author provides no information on origin, age, or sex for the single Cebus specimen he reports. (This reference is cited in Bauchot and Stephan, 1969.) Smith RJ (1980) Craniofacial morphology and diet of Miocene hominids. Ph.D. dissertation, Yale University. This reference is a secondary source. Spitzka EA (1903) Brain-weights of animals with special reference to the weight of the brain in the macaque monkey. J. Comp. Neurol. 13:9-17. The author states that most weights were taken from young individuals, many of which were emaciated and some also preserved. (This reference is cited in Bauchot and Stephan, 1969.) Takeshita H (1961-2) On the delivery behavior of squirrel monkeys (Saimiri sciureu) and a Mona monkey (Cercopzthecus mona). Primates 359-72. The weight of “about 600 g” (p. 6 0 ) for Saimiri sciureu [sic] appears to be a n estimate and not an actual weight. Warnke P (1908) Mitteilung neuer gihirn- und kor-

pergewichtsbestimmungen bei saugern, nebst zusammenstellung der gesamten bisher beobachteten absoluten und relativen gehirngewichte bei den verschiedenen spezies. J. Psychol. Neurol. 13:355403. It is unclear if the data are repeated in the several different tables, and if the data are original or from the literature. (This reference is cited in Bauchot and Stephan, 1969.) Weber M (1896) Vorstudien uber das hirngewicht der saugetiere. Festschrift zum siebenzigsten geburtstage von Carl Gegenbaur 21:105-123. The author includes weights of animals of all ages and varying nutritional states together in table and does not differentiate between them. (This reference is cited in Bauchot and Stephan, 1969.) Wettstein EB (1963) Variabilitat, Geschlechtsunterschiede, und Altersveranderungen bei Callithrk jucchus L. Morph. Jb. 104-2:185-271. Epple (1970) indicates that Wettstein’s weights ‘I. . . consisted mostly of probably malnourished animals who died during a transport from South America to Europe” (p. 71).

NOTES ADDED IN PROOF (1.)Body weight for Leontopithecus caissum is 572 g (female, one specimen): Locini ML and Persson VG, 1990, Nova especie de Leontopithecus Lesson, 1840, do sul do Brasil (Primates, Callitrichidae). Bol. Museu Nacional, n.s., 338:l-14. (2.) C. Cristoffer (1987) offers a n interesting speculation on the reasons behind the lack of very largebodied Neotropical primates: J. Biogeogr. 14:165-172. (Body size differences between New World and Old World, arboreal, tropical vertebrates: cause and consequences.)

Feeding adaptations in New World primates: an evolutionary perspective: introduction.

Evolution of feeding niches in New World monkeys.

Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae.

Brief Communication: Seasonality of diet composition is related to brain size in New World Monkeys.

Vertebral Adaptations to Large Body Size in Theropod Dinosaurs.

Contributions to the systematics of New World macro-moths VI.

Contributions to the systematics of New World macro-moths V.

Molecular variation in AVP and AVPR1a in New World monkeys (Primates, Platyrrhini): evolution and implications for social monogamy.

Laventiana annectens, new genus and species: fossil evidence for the origins of callitrichine New World monkeys.

Climatic niche evolution in New World monkeys (Platyrrhini).

S-cone visual stimuli activate superior colliculus neurons in old world monkeys: implications for understanding blindsight.

New Mitogenomes of Two Chinese Stag Beetles (Coleoptera, Lucanidae) and Their Implications for Systematics.

Chromosome size-correlated and chromosome size-uncorrelated homogenization of centromeric repetitive sequences in New World quails.

Growth in fossil and extant deer and implications for body size and life history evolution.

Body Size Adaptations to Altitudinal Climatic Variation in Neotropical Grasshoppers of the Genus Sphenarium (Orthoptera: Pyrgomorphidae).

Genetic diversity in oxytocin ligands and receptors in New World monkeys.

Lifespan, growth rate, and body size across latitude in marine Bivalvia, with implications for Phanerozoic evolution.

Evolutionary adaptations: theoretical and practical implications for visual ergonomics.

Patterns of MHC-G-Like and MHC-B Diversification in New World Monkeys.

Variation in ligand responses of the bitter taste receptors TAS2R1 and TAS2R4 among New World monkeys.

Neurotoxic amphetamine analogues: effects in monkeys and implications for humans.

Feeding adaptations in the hairs and tongues of nectar-feeding bats.

Short poly-glutamine repeat in the androgen receptor in New World monkeys.

Old world monkeys and new age science: the evolution of nonhuman primate systems virology.