AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 92:499-520 (1993)
Relative Growth of the Limbs and Trunk in Sifakas: Heterochronic, Ecological, and Functional Considerations
MATTHEW J. RAVOSA,DAVID M. MEYERS, AND KENNETH E. GLANDER Department of Cell, Molecular and Structural Biology, Northwestern University Medical School, Chicago, Illinois 60611 (M.J.R.); Department of Biological Anthropology and Anatomy (D.M.M., K.E.G.1 and Duke Uniuersity Primate Center (K.E.G.), Duke University, Durham, North Carolina 27706 KEY WORDS Propithecus, Allometryhcaling, Heterochrony, Ontogeny, Body proportions, Ecogeographic size variation, Sexual dimorphism
ABSTRACT Limb, trunk, and body weight measurements were obtained for growth series of Milne-Edwards’s diademed sifaka, Propithecus diadema edwardsi, and the golden-crowned sifaka, Propithecus tattersalli. Similar measures were obtained also for primarily adults of two subspecies of the western sifaka: Propithecus verreauxi coquereli, Coquerel’s sifaka, and Pro- pithecus verreauxi verreauxi, Verreaux’s sifaka. Ontogenetic series for the larger-bodied P. d. edwardsi and the smaller-bodied P. tattersalli were com- pared to evaluate whether species-level differences in body proportions result from the differential extension of common patterns of relative growth. In bivariate plots, both subspecies of P. verreauxi were included to examine whether these taxa also lie along a growth trajectory common to all sifakas. Analyses of the data indicate that postcranial proportions for sifakas are ontogenetically scaled, much as demonstrated previously with cranial dimen- sions for all three species (Ravosa, 1992). As such, P. d. edwardsi apparently develops larger overall size primarily by growing at a faster rate, but not for a longer duration of time, than P. tattersalli and P. verreauxi; this is similar to results based on cranial data. A consideration of Malagasy lemur ecology suggests that regional differences in forage quality and resource availability have strongly influenced the evolutionary development of body-size variation in sifakas. On one hand, the rainforest environment ofP. d. edwardsi imposes greater selective pressures for larger body size than the dry-forest environ- ment of P. tattersalli and P. u. coquereli, or the semi-arid climate of P. u. verreauxi. On the other hand, as progressively smaller-bodied adult sifakas are located in the east, west, and northwest, this apparently supports sugges- tions that adult body size is set by dry-season constraints on food quality and distribution (i.e., smaller taxa are located in more seasonal habitats such as the west and northeast). Moreover, the fact that body-size differentiation occurs primarily via differences in growth rate is also due apparently to differences in resource seasonality (and juvenile mortality risk in turn) be- tween the eastern rainforest and the more temperate northeast and west. Most scaling coefficients for both arm and leg growth range from slight negative allometry to slight positive allometry. Given the low intermembral
Received June 25,1992; accepted June 28, 1993 Address reprint requests to Dr Matthew J. Ravosa, Depart- ment of CMS Bioloby, Northwestern University Medical School, 303 E. Chicago Ave., Chicago, IL 60611.3008,
0 1993 WILEY-LISS, INC. 500 M.J. RAVOSA ET AL index for sifakas, which is also an adaptation for propulsive hindlimb-domi- nated jumping, this suggests that differences in adult limb proportions are largely set prenatally rather than being achieved via higher rates of postnatal hindlimb growth. Our analyses further indicate that the larger-bodied P. d. edwardsi has a higher adult intermembral index than P. tattersalli and P. uerreauxi, thus supporting the allometric argument regarding the interspe- cific scaling of limb proportions in arboreal primates which employ vertical postures (Cartmill, 1974,1985; Jungers, 1978,1985). Lastly, additional analyses indicate that P. d.edwardsi exhibits significant sexual dimorphism where adult females are larger than adult males in about one-third of all adult comparisons, whereas P. tattersalli exhibits significant sexual dimorphism in about one-fifth of all adult comparisons. Among west- ern sifakas, adult P. u. coquereli exhibit significant sex dimorphism in about one-third of all comparisons, whereas adult P. u. uerreauxi show no significant differences between the sexes. Given that all taxa are ontogenetically scaled, this suggests that sexual dimorphism develops via such processes as well. Interestingly, our data indicate that sex dimorphism is allometric, with larger-bodied taxa like P. d. edwardsi being more dimorphic. 0 1993 Wiley-Liss, Inc.
A number of recent allometric and hetero- trunk in lorisines, no other studies exist for chronic analysis have contributed much to strepsirhine primates. This is surprising be- our understanding of the developmental cause many strepsirhine congeners vary processes underlying patterns of ecogeo- considerably in body size (e.g., Albrecht et graphic size variation and phyletic size al., 1990; Kappeler, 1990, 1991; Glander et change in closely related primates. In Mala- al., 1992; Ravosa, 1992; Godfrey et al., gasy lemurs, Ravosa (1992) demonstrates 1993). that interspecific differences in adult skull Given a pervasive pattern of ontogenetic form among all three sifakas result from the scaling in two taxa of differing adult sizes, differential extension of common patterns of there are two options for the larger species allometric or relative growth. In other to evolve a larger terminal body size relative words, sifaka cranial morphology is ontoge- to the hypothetically ancestral or primitive netically scaled (sensu Gould, 1975) (Fig. 1). condition of the smaller species'. This is Little is known about ontogenetic scaling in commonly referred to as phyletic gigantism the postcranium of these primates, despite or peramorphosis via hypermorphosis that such methods are equally suited to ad- (Gould, 1977; Shea 1983, 1988). First, one dressing questions about locomotor form can examine rate of growth-in-time to deter- and function. mine whether the larger taxon grows faster In fact, apart from several early studies via rate hypermorphosis. That is, individu- regarding ontogenetic scaling of the anthro- als of the larger species develop progres- poid axial skeleton (e.g., Lumer, 1939; sively larger limb and trunk measures but Lumer and Schultz, 1941, 1947), similar al- mature at the same chronological age as lometric approaches to primate postcranial those of the smaller taxon (Fig. 2A). Second, morphology have been rare outside of the one can examine time of growth shut off to previous decade (e.g., Jungers and Fleagle, distinguish whether the larger taxon grows 1980; Shea, 1981, 1984, 1992; Buschang,
1982; Jungers and Susman, 1984; Jungers ~~ 'These scenarios assume no dissociation of allometric trajecto- et al., 1988; Jungers and Hartman, 1988; ries between species as is characterizedin the processes of accel- Falsetti and Cole, 1992; Gomez, 1992, in eration or neoteny (Shea, 1983,1988).Finally, these scenarios do press; Jungers and Cole, 1992). Moreover, not assume necessarily that both species have the same neonatal size,just that absolute differences in neonatal body size between except for Gomez's (1992, in press) studies species will be considerably less than interspecific differences in on growth and proportions of the limbs and adult body size. POSTCRANIAL GROWTH AND SCALING IN SIFAKAS 501
9: ONTOGENETIC SCALING & 8- PHYLETIC GIGANTISM ADULT SIZE OF LARGE TAXON to5; h 5- n ADULT SIZE OF 0 4- SMALL TAXON e4 3 3. COMMON I ' SIZEOF 2- NEONATES 1-
04. .., 0123456789 log BODY SIZE
Fig. 1. Growth trajectories for a measure of body shape vs. a measure of body size for two closely related species of differing adult sizes. Both taxa have similar growth allometries, such that morphological differences between adults of each species are due to the differential extension of shared patterns of relative growth (smaller-bodiedtaxon = solid square; larger-bodied taxon = open square). for a longer duration via time hypermorpho- to cases where the smaller-bodied taxon ma- sis. That is, members of the larger species tures at the same chronological age but have similarly sized extremities at the same grows at a slower rate than the larger-bod- subadult age as those of the smaller species ied taxon. Time hypomorphosis refers to but mature at a later chronological age (Fig. cases where the smaller-bodied taxon grows 2B) (Shea 1983,1988)'. Although considered at the same rage but for a shorter duration separately, it would be evident that both (Shea, 1983, 1988). As the polarity of size heterochronic processes affected the evolu- change among sifakas is presently un- tion of species differences in postcranial di- known, for the purposes of this study we mensions if developmental modifications oc- utilize terminology detailed in the previous cur early in ontogeny and become especially paragraph. marked in later stages. In this study, allometric analyses are ap- As a point of clarification, although the plied to ontogenetic series representing two body size and ontogenetic trajectory of the Malagasy primates of differing adult body smaller species may approximate more size: Propithecus diadema edwardsi (5,837 closely the ancestral or primitive pattern, g), Milne-Edwards's diademed sifaka from this is not always the case. Phyletic dwarf- the rainforest of Ranomafana, and Propithe- ing or paedomorphosis via ontogenetic scal- cus tattersalli (3,493 g), the golden-crowned ing would be an obvious exception to the sce- sifaka (Simons, 1988) from the dry forest of nario detailed above (Gould, 1977; Shea Daraina. The growth series are also com- 1983, 1988). In cases where the larger body pared to mostly adult data for two subspe- size more closely represents the primitive cies of Propithecus verreauxi, the western condition, the heterochronic terminology al- sifaka: Propithecus verreauxi coquereli ters accordingly. Rate hypomorphosis refers (3,992 g), Coquerel's sifaka from the dry for- est of Ankijabe and Propithecus uerreami verreauxi (3,098 g), Verreaux's sifaka from 'As used in this context, faster (rate) and longer (time) charac- terizations refer to growth-in-time, not to different coefficients the semi-arid forest of Bevola (Glander and (regressionslopes) of relative or allometric growth. Simons, in preparation). The allometric fo- 502 M.J. RAVOSA ET AL.
9. RATE HYPERMORPHOSIS & 8. ONTOGENETIC SCALING
7. 6- s-
4- 3. AGE 2 /I/ 2- U ANCESTRAL PATTERN PHYLETIC GIANT 1-
TIME HYPERMORPHOSIS & 8 ONTOGENETIC SCALING '1 AGF h
AGE 4 b 7 0 E9 M 3 -0 41 AGE 2 W ANCESTRAL PATTERN '1 AGE1 7 -tR PHYLETIC GIANT
Fig. 2. A larger-bodied species and a smaller-bodied species share similar growth trajectories for a measure of body shape vs. body size. The larger species can extend the smaller species' ontogenetic scaling trend to develop larger adult sizes in two manners. First, the larger species can grow faster via rate hypermorphosis (i.e., individuals of the same age are dissimilar in size but grow for the same amount of time) (A). Second, the larger species can also grow longer via time hypermorphosis (i.e., individuals of the same age are similar in size but grow for different durations) (B). On the other hand, if the growth pattern of the smaller species represents the derived condition, then the two heterochronic processes would be characterized, respectively, as rate and time hypomorphosis. cus of this study is fourfold: to evaluate vosa, 1992) morphology in sifakas, whether whether differences in limb and trunk pro- size differences among taxa develop via rate portions among congeners of differing body hypermorphosis, with P. d. edwardsi grow- size develop via ontogenetic scaling; to ad- ing faster, andor time hypermorphosis, dress, given a pervasive pattern of ontoge- with P. d. edwardsi growing longer; to de- netic scaling of postcranial and cranial (Ra- scribe the functional implications of limb POSTCRANIAL GROWTH AND SCALING IN SIFAKAS 503 and trunk growth in three species of vertical forest of northwest Madagascar by K.E.G. clingers and leapers; and lastly to highlight (1982, 1984). Additional limited ontogenetic the important link between patterns of in- data on body weight for 16 P. u. coquereli at tra- and interspecific scaling in the extremi- the DUPC were also considered, although in ties (e.g., Shea, 1981). only two cases do the data range from birth Considered more broadly, a heterochronic to adulthood. The sample of Verreaux’s si- analysis of the relative growth of sifaka body faka, Propithecus verreauxi uerreauxi, con- proportions has direct implications for mod- sists of seven adults that were trapped and els which stress the importance of ecological measured in the Bevola semi-arid forest of factors in the evolution of primate body size southwest Madagascar by K.E.G. (1984). In differences (e.g., Terborgh and van Schaik, all three species, several individuals were 1987; Albrecht et al., 1990). Therefore, an- measured more than once, such as at differ- other major focus of this study will be the ent times of the year or in successive years; ecological bases of size differentiation in si- therefore the growth series constitute fakas, since Milne-Edwards’s sifaka inhab- mixed-cross-sectional samples (Cock, 1966). its a rainforest environment, whereas the For between-species comparisons of si- golden-crowned sifaka and the western si- faka somatic development, the data are faka inhabit a dry-forest or semi-arid cli- grouped into six age classes based on half- mate. Lastly, this study will provide addi- year or yearly intervals as well as data tional data regarding sexual dimorphism in availability: 1 = 0-6 months; 2 = 6 sifakas, where adult females are larger than months-1.5 years; 3 = 1.5-2.5 years; adult males (Kappeler, 1990, 1991; Jenkins 4 = 2.5-4 years; 5 = 4-5 years; 6 = 5+ and Albrecht, 1991; Glander et al., 1992; Ra- years (adult). Chronological age for animals vosa, 1992; Godfrey et al., 1993). As such, in age classes 1-3 was often figured directly comparisons within and among these taxa or easily determined due to the highly sea- will further detail the developmental under- sonal nature of sifaka birth patterns. For pinnings of ecogeographic and sexual differ- older animals in age classes 4-6, the chrono- entiation in sifakas. logical age of several adults was estimated from tooth wear (Glander et al., 1992).In P. MATERIALS AND METHODS tattersalli there are at least four cases per age classes 1-5. The P. d. edwardsi sample Samples has at least four cases per age classes 1 and The ontogenetic sample of Milne-Ed- 5, only two cases for age classes 2 and 4, and wards’s diademed sifaka, Propithecus dia- three cases for age class 3. dema edwardsi, consists of 21 individuals (13 adults, 8 non-adults) that were trapped Measurements and measured in the Ranomafana rainforest Most morphometric data were obtained of southeast Madagascar by K.E.G. (May from individuals sedated and trapped in the 1987, 1988, 1989). The ontogenetic sample field. Body weights were taken by suspend- of the golden-crowned sifaka, Propithecus ing infants from a 1 kg portable spring scale tattersalli, consists of 40 individuals (18 and adults from a 20 kg portable spring adults, 22 non-adults) that were trapped scale; weights were recorded to within 10 g and measured in the Daraina dry forest of (Glander et al., 1991, 1992). Neonate and northeast Madagascar by D.M.M. (1989, infant body weight data for P. tattersalli and 1990). Limited body weight data from birth P. u. coquereli at the DUPC were collected to adulthood for one P. tattersalli at the using a 1kg triple-beam scale; no other data Duke University Primate Center (DUPC) were available for DUPC sifakas. In addi- were also included. Adult data for two sub- tion to body weight, eight linear and three species of the western sifaka, Propithecus circumferential measures were taken on uerreawi, were also obtained. The sample of wild-caught animals (SeeAppendix A at end Coquerel’s sifaka, Propithecus uerreawi co- of text). These data were recorded to the quereli, consists of 15 adults that were nearest millimeter with a 3 meter metal trapped and measured in the Ankijabe dry tape and are defined according to Glander et 504 M.J. RAVOSA ET AL.
6.41
6.2. H
17 UU 2 5.8- W il $I 5.6- n 0 Ep 5.4. 17 2 5.2. nu H P.D.EDWARDS1 0 P.VERREAUX1 5-
4.8. . .
LOG BODY WEIGHT
Fig. 3. A plot of log, body length (mm)vs. log, body weight (g). Note that the growth series for all three sifakas species are coincidental, such that morphological differences between adults are due to the differential extension of shared scaling patterns. This typifies the majority of sifaka comparisons.
al. (1991, 1992). Three additional linear vidual values suggest that this may not be a measures were derived from the original major consideration for sifakas (e.g., Figs. data: body length, arm length, and leg 3-61. length. Upper arm and thigh circumference Body weight was used as the independent were not collected for western sifakas. variable in most bivariate comparisons, al- though several additional comparisons were Statistical analyses made, such as arm length vs. leg length. Within both ontogenetic series, least- While isometry in bivariate comparisons be- squares and reduced major-axis bivariate tween linear measures is a slope value of regression analyses (P < 0.05) were applied 1.00, in cases where linear measures are to log-transformed morphogenic data to de- regressed against body weight isometry scribe allometric growth trajectories. Fol- equals 0.33. When a circumferential mea- lowing Sokal and Rohlf (19811, the standard sure is compared to body weight an isomet- error of the least-squares slope is used for ric slope equals 0.67, and when a circumfer- the reduced major-axis slope as well. For re- ential measure is compared to a linear gression analyses in both growth series the measure isometry equals a value of 2.00. data were averaged by age class and sex, in Analysis of covariance (ANCOVA) (P < large part so as to reduce the effects of dis- 0.05) was used to test for differences in pat- proportionately large numbers of cases in a terns of relative growth between least- particular age class or sex on the slope of the squares regression lines derived for each regression line. For example, since adults lie growth series, namely whether sifakas are at one end of the size range, greater num- ontogenetically scaled. bers of adults would bias the calculation of As only adult limb and trunk data are the regression line and thereby potentially available for both P. u. coquereli and P. u. result in a lower regression coefficient. To be uerreauxi, an alternative method was used sure, it is possible that grouping the data by to assess whether these taxa are ontogeneti- age group may mask more complex allomet- cally scaled versions ofP. d. edwardsi and P. ric patterns; visual inspections using indi- tattersalli. In this case, if the postcranial POSTCRANIAL GROWTH AND SCALING IN SIFAKAS 505
6- z
z 0 2 5- 4.8- P.D.EDWARDS1 2 0 P.VERREAUX1 4.6-
4.4- . .
Fig. 4. A plot of log, forelimb length vs. log, body weight. As in most comparisons, the ontogenetic scaling trajectory for Milne-Edwards’s sifaka, that for the golden-crowned sifaka, and the adult data for both subspecies of the western sifaka are coincidental.
6.2. - ’
6- 5.8- z b 5.6- 19 5 5.4- c;l CI 5.2-
c3 5- CI 0 0 4.8- CI c;) 4.6. W P.D.EDWARDS1 0 P.VERREAUXI 4.4- W 4.27 c
Fig. 5. A plot of loge leg length vs. log, arm length. Again, the data for all three species lie along a common ontogenetic trajectory.
growth trajectories for Milne-Edwards’s si- netically scaled (see Ravosa, 1992; Shea, faka and/or the golden-crowned sifaka inter- 1992; also Jungers and Cole, 1992). How- sect the adult scatter for either subspecies of ever, if the adult data scatter fall mostly the western sifaka, then it is most parsimo- above or below the regression line, then it is nious to infer that these forms are ontoge- inferred that morphological differences be- 506 M.J. RAVOSA ET AL. t m. mm
P.DIA DEMA
-1 -100 100 200 300 400 500 600 700 800 9001 k AGE (weeks) Fig. 6. A plot of body weight vs. age (weeks). Note that individual wild-caught and DUPC data for all taxa lie along the same growth curve early in ontogeny. Sifaka growth patterns differ only at later ontogenetic stages due to terminal differentiation in adult body size among species. tween adults of each sister taxon do not re- would indicate that species differences in sult from the differential extension of com- body size develop via rate hypermorphosis mon patterns of relative growth. (Shea, 1983,1988);that is, the larger-bodied T-tests (P < 0.0513 were used to examine Milne-Edwards’s sifaka grows at a faster species and sex differences in postcranial di- rate, but not for a longer period of time than mensions at similar age classes. For in- the golden-crowned sifaka (Ravosa, 1992). stance, given a pervasive pattern of ontoge- On the other hand, if species differences are netic scaling among sifakas, if at common noted only between adult sifakas, then this age classes subadult means for each vari- would indicate that morphological differ- able are significantly different, then this ences develop via time hypermorphosis (Shea, 1983,1988); that is, Milne-Edwards’s sifaka grows for a longer duration, but not at a faster rate than the smaller-bodied golden- ’In both between-species and between-sex analyses, compari- crowned sifaka (Ravosa, 1992). These pat- sons are made with “original” measures (e.g., tail length), “origi- terns of growth increases are not mutually nal composite” measures (e.g., tail-crown length), and “derived measures (e.g., body length). This may lead to a potential bias in exclusive, however. For example, if slight accepting greater numbers of significant or non-significant com- body-size differences are noted early in on- parisons, as the original composite and/or derived measures may togeny and are more marked between adult not necessarily vary independent of the original measures. In this study, such a pattern does not seem to characterize the sifakas, then this would suggest that size majority of sifaka comparisons. differentiation evolved by P. d. edwardsi POSTCRANIAL GROWTH AND SCALING IN SIFAKAS 507 TABLE I. Propithecus tattersalli bivariate reeression analvses Vs. body weighP3 Y-int Slope 95% CI Body length 3.397 0.320 20.025 0.974 3.328 0.329 Tail-crown length 4.063 0.330 k0.024 0.976 4.003 0.338 Tail length 3.387 0.334 t0.033 0.958 3.268 0.349 Chest circumference 2.600 0.374 +0.037 0.958 2.473 0.390 Forelimb length 3.226 0.312 k0.022 0.979 3.175 0.319 Forefoot length 2.334 0.282 kO.021 0.977 2.279 0.289 Arm length 2.719 0.327 20.024 0.977 2.660 0.335 Thumb length 1.127 0.337 20.023 0.980 1.075 0.344 Upper arm circumference 1.667 0.371 k0.042 0.946 1.503 0.392 Hindlimb length 3.716 0.300 %0.018 0.984 3.674 0.305 Hindfoot length 2.712 0.276 k0.025 0.966 2.632 0.286 Leg length 3.270 0.310 %0.018 0.985 3.234 0.315 Big-toe length 2.495 0.235 k0.023 0.961 2.418 0.245 Thigh circumference 1.433 0.460 *0.019 0.992 1.389 0.466
Forelimb vs. hindlimb length -0.607 1.036 20.055 0.988 -0.687 1.049 Arm length vs. leg length -0.684 1.047 -t0.064 0.984 -0.782 1.064 Upper arm vs. thigh circumference 0.531 0.802 20.089 0.949 0.315 0.845 Upper arm vs. arm length -1.526 1.112 ?0.150 0.923 -1.793 1.205 Thigh circumference vs. leg length -3.274 1.458 t0.070 0.990 -3.359 1.473 'All of the regression analyses are performed on pooled-sex samples. 2Most regression slopes are significantly different from zero at P < 0.01; the rest are significant at P < 0.05. In all hivariate comparisons, least-squares regression analyses are indicated on the first line, while reduced major-axis regression analyses are indicated second.
growing both faster and for a longer period for most limb and trunk measures. In 17 of of time. 19 cases, between-species comparisons RESULTS (ANCOVAs) of postcranial growth patterns are not significantly different between P. Ontogenetic scaling in sifakas tattersalli and P. d. edwardsi (Table 3). In Propithecus tattersalli all 14 bivariate When the mostly adult data for Propithecus regressions vs. body weight, as well as the uerreauxi coquereli and Propithecus uer- five additional comparisons, are highly cor- reauxi uerreauxi are plotted with the two related (Table 1). In Propithecus diadema growth series, 12 of 14 comparisons likewise edwardsi all 14 bivariate regressions vs. cluster along common scaling trajectories body weight, as well as the five additional (Table 3; Figs. 3-6). Among all three species, comparisons, are moderately to highly cor- the cases that do not indicate ontogenetic related (Table 2). The regression coefficients scaling are hindfoot length (Fig. 7) and tail for both species typically indicate slight neg- length (Fig. 8) vs. body weight (Table 3). ative allometry to slight positive allometry Therefore, the vast majority of morphologi- 508 M.J. RAVOSA ET AL.
TABLE 2. Propithecus diadema edwardsi bzuariate regression analyses Vs. body Y-int Slope 95% CI r Body length 3.323 0.330 c0.012 0.994 3.308 0.332 Tail-crown length 3.730 0.362 20.013 0.995 3.714 0.364 Tail length 2.695 0.400 20.022 0.988 2.657 0.405 Chest circumference 1.953 0.451 t0.088 0.889 1.479 0.507 Forelimb length 2.697 0.381 20.012 0.996 2.678 0.383 Forefoot length 2.001 0.337 t0.009 0.997 2.991 0.338 Arm length 2.054 0.407 A0.017 0.993 2.027 0.410 Thumb length 1.462 0.309 A0.025 0.975 1.406 0.316 Upper arm circumference 2.482 0.284 k0.105 0.715 1.524 0.397 Hindlimb length 2.945 0.395 ?0.013 0.996 2.927 0.397 Hindfoot length 2.551 0.306 t0.012 0.994 2.534 0.308 Leg length 2.122 0.447 20.015 0.996 2.104 0.449 Big-toe length 1.629 0.352 t0.018 0.990 1.593 0.356 Thigh circumference 1.295 0.474 -t0.048 0.967 1.159 0.490
Forelimb vs. hindlimb length -0.136 0.963 10.015 0.999 -0.142 0.964 Arm length vs. leg length 0.123 0.910 t0.021 0.998 0.112 0.912 Upper arm vs. thigh circumference 1.678 0.604 20.204 0.746 0.586 0.810 Upper arm vs. arm length -1.907 1.204 20.354 0.834 -3.054 1.444 Thigh circumference vs. leg length -3.421 1.478 -t0.188 0.948 -3.907 1.560 'All of the regression analyses are performed on pooled-sex samples. 'Most regression slopes are significantly differentfrom zero at P < 0.01, the rest are significant at P i0.05. 31n all bivariate comparisons,least-squares regression analyses are indicated on the first line, while reduced major-axis regression analyses are indicated second.
cal differences between adults are due to the size. This pattern is also demonstrated at differential extension of common patterns of age class 5, where 14 of 15 comparisons are relative growth. In other words, limb and significantly different, and at age class 4, trunk proportions for Milne-Edwards's si- where 11 of 15 T-tests are significant. Like- faka, the golden-crowned sifaka, and the wise, this is indicated to a lesser extent at western sifaka are ontogenetically scaled age class 3, where 9 of 15 comparisons are (much as found in the skull for these taxa significantly different. At age class 2, only [Ravosa, 19921). three significant differences are noted be- tween sifaka postcranial measurements. Al- Growth and size differentiation in sifakas though not always statistically significant At age class 6, T-tests for limb, trunk, and at age class 2, 100% of the means for P. d. body weight dimensions between P. d. ed- edwardsi measures exceed the means for P. wardsi and P. tattersalli are significant in tattersalli measures. This pattern of body- all 15 cases (Table 4); that is, adult Milne- size enlargement is maintained at later Edwards's sifakas are consistently larger in stages in ontogeny as well. While similar POSTCRANIAL GROWTH AND SCALING IN SIFAKAS 509
TABLE 3. Between-species ANCOVAs for both sifakas are consistantly larger except in growth series and tests of positional differences for all three suecies comparisons of tail length, where western sifakas are significantly larger, and tail- Variable’ - Vs. body weight’ crown length, where P. d. edwardsi only Body length NS tends to be larger (i.e., differences exist Tail-crown length NS Tail length D < T < V3,4 which are not statistically significant). At Chest circumference NS age class 6, T-tests for limb, trunk, and body Forelimb length NS weight dimensions between P. tattersalli Forefoot length NS Arm length NS and P. verreauxi are significant in only 4 of Thumb length NS 13 cases (Table 5). In this suite of analyses, Upper arm circumference NS golden-crowned sifakas are significantly Hindlimb length NS Hindfoot length D > T > V4,5 larger in chest circumference and hindfoot Leg length NS length and tend to be larger in body length, Big-toe length NS Thigh circumference NS forelimb length, forefoot length, arm length, hindlimb length, and big-toe length. On the Forelimb length vs. hindlimb NS other hand, western sifakas are signifi- length Arm length vs. leg length NS cantly larger in tail length and tail-crown Upper arm circumference vs. thigh NS length and tend to be larger in body weight, circumference thumb length, and leg length. Upper arm circumference vs. arm NS length Thigh circumference vs. leg leneth NS Sexual dimorphism in sifakas ‘No data are available for analyses of upper arm or thigh circumfer- Based on 15 limb, trunk, and body weight ence in P. uerreauxi. ‘NS = no significant differences between sifaka regression lines, measures, adult P. d. edwardsi (9 females, P > 0.05, and no differencesbetween the position of the adult data 10 males) show significant sexual dimor- scatter for P. uerreawi wlth respect to the regression lines. 3Significant slope and Y-intercept differencesbetween sifaka least- phism where females are larger than males squares regression lines, ANCOVA (P < 0.05). D > T > V means P. d. edwurdsi regression line is transposed above in body weight, tail-crown length, tail the P. tattersalli line, which is in turn transposed above the adult P. length, body length, and hindfoot length uerreauxi data scatter; D > T > V means P. uerreawli adult data scat- ter is transposed above the P. tattersalli regression line, which is in (Table 6). Our results also indicate that turn transposed above the P. d. edwardsi line adult P. tattersalli (10 females, 8 males) ’Significant Y-intercept differences between sifaka least-squares re- gression lines. show significant sex dimorphism in tail- crown length, body length, and forefoot length. The results further demonstrate that adult P. v. coquereli (5 females, 10 analyses were not possible for all measures males) show significant sex dimorphism in at age class 1, based on body weights alone, body weight, leg length, hindlimb length, P. d. edwardsi (wild-caught), P. tattersalli and forefoot length. Lastly, our results for (DUPC), and P. v. coquereli (DUPC) have adult P. u. verreauxi (4 females, 3 males) do fairly similarly sized neonates ranging in not indicate significant sexual dimorphism size from 84 to 155 g4. in any of 13 measures. In fact, female mea- At age class 6, T-tests for postcranial and sures do tend to be larger in 6 of 13 compari- body weight measures between P. d. ed- sons, whereas male measures tend to be wardsi and P. verreauxi are significant in 12 larger in six cases (Table 6). of 13 cases (Table 5). Adult Milne-Edwards’s DISCUSSION Allornetry and heterochrony in sifakas ‘Based on two wild-caught individuals, P. d. edwardsi has an average “neonate”weight of 145 g. Based on 1 DUPC individual, Propithecus diadema edwardsi, Propithe- P. tattersalli has a neonate weight of 98 g. Based on 12 DUPC cus tattersalli, Propithecus verreauxi coquer- individuals, P. u. coquereli has an average neonate weight of 105 eli, and Propithecus verreauxi verreauxi g. The range for P. u. coquereli (84-129 g) includes the P. tutter- sulli value and falls just below that for P. d. edwurdsi (135 and share common patterns of relative growth in 155 g). However, whereas the data for DUPC sifakas were col- the limbs and trunk (Table 3; Figs. 3-61, as lected on the day of birth, the Milne-Edwards’s sifaka data were collected at least several days after birth, resulting in elevated well as in the skull and jaws (Ravosa, 1992). values for “neonate” weight. Our analyses suggest that P. d. edwardsi 510 M.J. RAVOSA ET AL.
5.41 t I z 5.2- a 5- Ec;i b 4.8- 0 0 4.6- 0 i5 0 3: 4.4- 0 0 n P.D.EDWARDSI 0 P.VERREAUXI rl 4.2- 0 W 4.. 5 5.5 6 6.5 7 7.5 8 8.5 9t LOG BODY WEIGHT
Fig. 7. A plot of log, hindfoot length vs. log, body weight. Note that the ontogenetic scaling trajectory for P. tattersalli does not intersect the scatter for P. d. edwardsi or P. uerreauxi. Instead, the growth pattern for Milne-Edwards’s sifaka is transposed above that for the golden-crowned sifaka and the adult data for western sifakas. These scaling differences are perhaps linked to functional differences in locomotor behavior due to interspecific variation in adult size. attains larger adult body size mainly by later stages of ontogeny (Shea, 1983, 1988; growing at a faster or higher rate than P. Ravosa, 1992). However, if the polarity of tattersalli (and P. uerreauxi) (Table 4). For size change were reversed, golden-crowned instance, this is evident in the patterns of sifakas would be considered to have at- weight increases for P. d. edwardsi and P. tained smaller body size via rate hypomor- tattersalli. At 1 year of age, juvenile P. d. phosis. In fact, species differences appar- edwardsi weight on average 2,950 g, which ently occur early in postnatal development, amounts to 51% of the average adult weight since by age class 2 all P. d. edwardsi mea- of 5,837 g. At 1year of age, juvenile P. tatter- sures at least tend to be larger than those for salli weigh on average 2,384 g, which P. tattersalli (Table 4). This corresponds amounts to 68% of the average adult weight closely to a similar analysis of allometry and of 3,493 g. Thus in Milne-Edwards’s sifaka, heterochrony in the sifaka cranium. That is, whereas a lesser percentage of the adult the majority of dimensions for all three si- body weight is attained by 52 weeks, this fakas are ontogenetically scaled and P. dia- amounts to an absolutely greater increase in dema develops larger adult skull size than body weight because P. d. edwardsi weighs P. verreauxi and P. tattersalli via rate hyper- more and gains more weight in 1 year than morphosis (Ravosa, 1992). One reason why the golden-crowned sifaka. rate hypermorphosis is perhaps more impor- Therefore, if the smaller overall adult size tant than time hypermorphosis in the devel- and the ontogenetic trajectory of the golden- opment of sifaka body-size differentiation is crowned sifaka (and western sifaka) more that data on populations of P. d. edwardsi, closely approximate the primitive condition P. tattersilli, P. u. coquereli, and P. u. uer- for Propithecus, then the growth pattern for reauxi (for P. u. uerreauxi, see also Richard Milne-Edwards’s sifaka follows the predic- et al., 1991) indicate that sexual maturity is tion for rate hypermorphosis because signif- reached at approximately the same age of icant differences in the size of postcranial 4-5 years old (also Ravosa, 1992; Meyers measures become more expressed in the and Wright, 1993). POSTCRANLAL GROWTH AND SCALING IN SIFAKAS 511
6.4
6.2 5 6 0 5.8 z 2 5.6 $ 5.4 t3 0 5.2 0
45 W P.D.EDWARDSI 4.8
4.6 5 5.5 6 6.5 7 7.5 8 8.5 9 LOG BODY WEIGHT
Fig. 8. A plot of log, tail length vs. log, body weight. Note again that the ontogenetic scaling trajectory for P. tattersalli does not intersect the scatter for P. d. edwardsi or P. uerreauxi. Rather, the data for adult western sifakas are transposed above the scaling trajectory for the golden-crowned sifaka and that for Milne-Edwards's sifaka.
TABLE 4. Between-species T-tests at each age class tion among all Malagasy lemurs or primates (see also Godfrey and Petto, 1981; Godfrey P. d. edwardsi vs. Variable P. tattersalli l4 et al., 1990).They found a consistent pattern of adult size differences among sister taxa Hindfoot length Forefoot length such that the largest forms were found in Hindlimb length the central domain and progressively Body weight smaller-bodied taxa were located respec- Leg length Forelimb length tively in the east, west, north, and south. Thumb length Differences in resource productivity among Big-toe length Thigh circumference ecogeographic regions were suggested to be Body length potential causes of this pattern, with the dry Upper arm circumference southern forests supposedly containing the Arm length Tail-crown length poorest food productivity and the central Chest circumference plateau having the highest productivity (at Tail leneth least until the recent past). Sifakas provide 'Age classes 24: cases where P. d. edwardsi measures are signifi- an interesting test of models of ecogeo- cantly larger than P. tattersalli are noted in bold; otherwise, the T-tests are not significant (P> 0.05). graphic variation since differences in adult 'Variables are ranked in ascending order by the age class at which size are due to ontogenetic scaling (Ravosa, species differences in bold develop. 3Not enough data spanning the entire range of age class 1 are avail- 1992) and different taxa inhabit several eco- able for T-tests at age class 1; however, baaed on wild-caught and DUPC data for all three species, there are no apparent differencesin geographic regions: P. diadema is located in body weight at age class 1 (see also text). the moist eastern rainforests, P. uerreauxi is 4By age class 2, though not always statistically significant, 100% of the means for P. d. edwardsi measures exceed the means for P. tatter- found in the dry northwest and semi-arid salli measures; in fact, this pattern of body size enlargement is main- southwest, and P. tattersalli is located in the tained through adulthood. dry northeast. In this section we address how ecological factors may influence pat- Ecological bases of body size variation terns of body-size differentiation among si- in sifakas fakas and other Malagasy lemurs. In particu- Albrecht et al. (1990) recently described a lar, two alternative models regarding body- pervasive trend in ecogeographic size varia- size variation are considered: adult body 512 M.J. RAVOSA ET AL.
TABLE 5. Between-species T-tests at adulthood P. d. edwardsi vs P. d. edwardsi vs P. tattersalli vs. Variable',' P. tattersalli3 P. uerreauxi4 P. uerreauxi5 Body weight D>T D>V T
TABLE 6. Between-sex T-tests at adulthood
Variable 1-3 P. d. edwardsi P. tattersalli P. u. coquereli P. u. uerreaui Body weight F>M F>M F>M F
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