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Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2010)

RESEARCH

PAPER

(Global Ecol. Biogeogr.) (2010) RESEARCH PAPER One size does not fit all: no evidence for an

One size does not fit all: no evidence for an optimal body size on islands geb_531 1

Pasquale Raia 1,2 *, Francesco Carotenuto 1 and Shai Meiri 3

10

1 Dipartimento di Scienze della Terra, Università Federico II, Largo San Marcellino 10, 80138 Naples, Italy, 2 Center for Evolutionary Ecology, Largo San Leonardo Murialdo 1, 00146 Roma, Italy, 3 Department of Zoology, Tel Aviv University, Tel Aviv 69978, Israel

*Correspondence: Pasquale Raia, Dipartimento di Scienze della Terra, Università Federico II, Largo San Marcellino 10, 80138 Naples, Italy. E-mail: pasquale.raia@libero.it

ABSTRACT

Aim Optimal body size theories predict that large clades have a single, optimal, body size that serves as an evolutionary attractor, with the full body size spectrum of a clade resulting from interspecific co mpetition. Because interspecific competi- tion is believed to be reduced on islands, such theories predict that insular animals should be closer to the optimal size than mainland animals. We test the resulting prediction that insular clade members should therefore have narrower body size ranges than their mainland relatives.

Location World-wide.

Methods We used body sizes and a phylogenetic tree of 4004 mammal species, including more than 200 species that went extinct since the last ice age. We tested, in a phylogenetically explicit framework, whether insular taxa converge on an optimal size and whether insular clades have narrow size ranges.

Results We found no support for any of the pre dictions of the optimal size theory. No specific size serves as an evolutionary attractor. We did find consistent evidence that large (> 10 kg) mammals grow smaller on islands. Smaller species, however, show no consistent tendency to either dwarf or grow larger on islands. Size ranges of insular taxa are not narrower than expected by chance given the number of species in their clades, nor are they narrower than the size ranges of their mainland sister clades – despite insular clade members showing strong phylogenetic clustering.

Main conclusions The concept of a single optimal body size is not supported by the data that were thought most likely to show it.We reject the notion that inclusive clades evolve towards a body-plan-specific optimum.

Keywords Body size evolution, Brownian motion model, island rule, mammalian phylogenetic tree, optimal body size theory, phylogenetic dispersion.

INTRODUCTION

Optimal body size theory (hereafter OST) suggests that large clades (e.g. mammals) have a fundamental size at which fitness is maximized (Maiorana, 1990; Brown et al., 1993). In mammals this size was claimed to be 100 g, based on interspe- cific allometries of resource acquisition and reproduction (Brown et al., 1993), although a different optimum (1 kg), based on a different model, was empirically estimated by Damuth (1993). The applications of the OST have been extended to birds and snakes, although an optimal size based on fitness estimates (33 g) has been calculated only for birds (Maurer, 1998).

© 2010 Blackwell Publishing Ltd

Brown et al. (1993) asserted that the OST explains the global body size frequency distribution of terrestrial mammals which, they claimed, shows a strong mode near 100 g. Moreover, they stated that the OST explains the tendency of small mammals to grow large and of large mammals to grow small on islands (i.e. the ‘island rule’; Van Valen, 1973). Interspecific competition was the only force suggested to keep species away from the body size optimum. Brown et al. (1993) and Damuth (1993) hypothesized that on islands, where faunas have few species, interspecific competition is reduced and species are free to evolve towards their optimal size, driving the island rule. Although simple and intuitively appealing, the OST has received as much criticism as support. Optimal size theory was

DOI: 10.1111/j.1466-8238.2010.00531.x www.blackwellpublishing.com/geb

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P. Raia et al.

claimed to be based on unrealistic parameters (Kozlowski, 1996), to mix reproductive output and conversion rate (Perrin, 1998), individual with population estimates (Kozlowski & Gawelczyk, 2002) and be inherently inconsistent (Bokma, 2001; cf. Brown et al., 1996). Empirically, the OST failed to predict the allometric scaling of life-history traits in bats (Jones & Purvis, 1997; Purvis, 2006) and insectivores (Symonds, 1999), the mass distributions of Australian marsupials (Chown & Gaston, 1997), and the rela- tionships between body size and home range in strepsirhine monkeys (Lehman et al., 2007). On conceptual grounds, the existence of a single optimal size at 100 g implies that all members of successful mammalian clades such as artiodactyls and carnivores are suboptimally sized, which is a contentious assertion (Blackburn & Gaston, 1996; Meiri et al., 2005). Within the realm of island biogeography, the evidence for OST is usually estimated from the relationship between body size range and island area: the body sizes of the smallest species on each island are regressed against island area (a proxy for species richness), and so are the body sizes of the largest species on each island (see, e.g., Marquet & Taper, 1998, Fig. 1; Boback & Guyer, 2003, Fig. 2; Meiri et al., 2005, Fig. 2). OST predicts that the intersection of these two regression lines will occur near the optimal size. Larger islands may contain more extreme sizes by chance alone, as more species are ‘drawn’ from the species pool (Marquet & Taper, 1998). Thus the regression lines will always intersect at some small island area value, and, by chance, this area would probably correspond to a body size near the taxon mode. We therefore argue that it is reasonable to assume that, under the OST, the true intersection should be nearer to the optimum than a random draw of species from a global pool according to the richness on each island. The intersection of such regression lines was near the putative 100 g optimal size of terrestrial mammals (Marquet & Taper, 1998) and near the modal size of snakes (0.88–1.08 m; Boback & Guyer, 2003). Interestingly, however, the intersection of the regression lines for snakes (1.22 m) was further away from the modal size than randomized data (0.92 m, Boback & Guyer, 2003). Likewise, for mammals, Marquet & Taper (1998) found that mass at the regression line intersection (51 g) was signifi- cantly lower than expected by chance (100–112 g), and thus also lower than the supposed 100 g optimum. For insular carnivores Meiri et al. (2005) found that the actual regression line intersec- tion (4363 g) was far from 100 g, and significantly higher (i.e. further away from 100 g) than the null (3122 g). Thus island biogeographic data seem to show that animals on species-poor islands have non-random body sizes, but not necessarily close to the putative optimal size of a clade. The OST was further invoked to explain body size patterns in insular turtles and bats (Lomolino, 2005), but failed to explain size evolution of large herbivores and carnivores (Raia & Meiri, 2006). Lomolino (2005) did not directly test the OST, but claimed nonetheless that his data (for reptiles, mammals and birds) are consistent with the notion that an optimal size drives the island rule. He argued, however, that multiple optimal body sizes exist, and suggested optima are body-plan specific.

Because adherents of the OST claim deviations from optimal- ity are the result of interspecific competition (only) they predict that insular mammals, especially on small islands, should often converge on the optimum. The optimal size is therefore an evo- lutionary attractor. At least two explicit tests of the existence of an evolutionary body size attractor (although neither used insular animals) were presented: Alroy (1998) used putative ancestor–descendant relationships of North American Cenozoic mammals. He found no evidence that the 100 g body size was an evolutionary attractor. Roy et al. (2000) found remarkably con- sistent modes and medians in body size frequency distributions of four assemblages of marine bivalve species along a latitudinal gradient in the north-eastern Pacific continental shelf. Yet, using fossil data, they found no evidence that bivalve genera evolved toward any optimal size. We contend that the OST predicts that size ranges on islands will be narrow, because this theory assumes many insular species encounter little competition, and are thus free to evolve towards the optimum. Some theory of community assembly, however, predicts that much of the size range will be present even at relatively low richness: Brown & Nicoletto (1991) and Cardillo (2002) have shown that species-poor assemblages often have similar size ranges to species-rich ones, with a size frequency distribution tending towards log-uniformity in the former versus log-normal or even a right-skewed distribution in the latter. Species-rich assemblages mostly differ from species-poor ones because they contain more modal-sized species (Olson et al., 2009). Thus OST will predict that size ranges will be more restricted on islands than expected if insular species are a random sample of the global species pool. If even species-poor assemblages cover much of the size range, however, insular species will have wider size ranges than expected under such a naïve null (Meiri & Thomas, 2007). Body size is often evolutionarily conserved. Thus, if insular taxa are phylogenetically closely related, then they are likely to have a more restricted size range than a random group with the same number of species on the mainland. A relevant null hypothesis should therefore account for phylogenetic relation- ships, because the OST predicts that stabilizing selection for the optimal size does occur. This implies that insular species will be more similar to each other than expected under the Brownian motion model of evolution (i.e. they should evolve body size conservatism and not just show a phylogenetic signal in body size; Losos, 2008). The Brownian motion model is one, and the simplest, of a class of models proposed to account for non- independence of species trait data due to shared ancestry (Freckleton et al., 2002). In it, the expected phenotypic diver- gence between species is proportional to the time since their divergence. More complex models can account for an ‘early burst’ (i.e. non-gradual) mode of trait evolution, or test for the existence of adaptive peaks (Lavin et al., 2008). The evolution of mammalian body sizes in the class as a whole probably differs from a Brownian motion-like body size evolution in being partly punctuational (Mattila & Bokma, 2008). Furthermore, ecologi- cal components such as character displacement, species sorting in local assemblages, or clinal adaptation to environmental con-

ditions (e.g. Bergmann’s rule) are known to affect the variance in body size in mammals even after the effect of phylogeny (i.e. shared ancestry) is accounted for (Diniz-Filho & Bini, 2008; Diniz-Filho et al., 2009). The Brownian motion model, however, is an unbiased depiction of size evolution. It is free from assumptions regarding the direction of natural selection, and therefore provides a convenient null to test for the occurrence of selection for an optimal size as predicted by the OST. Here we explicitly test two predictions of OST: that insular species evolved toward the 100 g body size optimum and that body size range is narrower in insular taxa than expected by chance. Using a relatively complete body size dataset and phy- logeny for mammals, we test whether the median size of insular clades is closer to 100 g, as per Brown et al. (1993), or to 1 kg, as per Damuth (1993), and other possible values (see below) than the body size of species in their mainland sister clades. We further test whether the size ranges of the insular clades are narrower than those of their mainland sister clades controlling for clade richness. We compare size ranges in insular clades with those produced by simulations performed under the Brownian motion model of evolution. Finally, we estimate whether the size range computed over all insular endemic species within a family is narrower than expected by chance, after controlling for species richness.

MATERIALS AND METHODS

Phylogenetic and body size data

To test the predictions of OST using phylogenetically informed null models, we modified the mammal species-level phyloge- netic tree published by Bininda-Emonds et al. (2008). We omitted marine mammals (cetaceans, sirenians and pinnipeds) and species for which we had no body size data. The modified tree includes 4004 extinct and extant mammal species. Body masses were taken from Smith et al. (2003) and additional sources (see Appendix S1A in Supporting Information). Insu- larity data are from Smith et al. (2003), verified using multiple sources. Body size (in grams) was log 10 transformed in all analyses. Human activity drove many insular mammals to extinction (e.g. Diamond, 1982). Alcover et al. (1998) estimated that 27% of insular endemic mammals have gone extinct since human colonization of their islands. Human-driven extinctions on the continents were no less severe. Worse, extinctions were strongly size-biased (i.e. most extinctions were of large mammals; e.g. Johnson, 2009). Thus, comparing mammal sizes on islands and the mainland may be biased by poor and non-random sampling. Consequently, we included all species known to have gone extinct since the final part of the last glacial phase (some 40,000 yr bp), for which a consistent body mass estimate and a clear phylogenetic hypothesis were both available. We thus restricted ourselves to species that were still living when human activities began to affect mammalian faunas world-wide (Johnson, 2009). These extinct species include disparate taxa such as marsupials, ungulates, xenarthrans, bats and rodents

No optimal body size in mammals

(Appendix S1A). Thus, it is reasonable to assume that our sample of extinct taxa is unbiased in relation to body size or taxonomy. Body masses for extinct taxa, their status as insular endemics and the works used to reconstruct their phylogeny and body sizes are reported in Appendix S1. To produce our phylogenetic tree, we used the branch lengths reported in Bininda-Emonds et al. (2008). For extinct taxa we used estimated age of separation (split age) between

fossil taxa as reported in the source papers if available (Appen-

dix

S1). Otherwise, we assessed the split age between sister taxa

by

using their oldest fossil occurrence reported in The Paleo-

biology Database (http://paleodb.org/cgi-bin/bridge.pl). Where

no

precise temporal reference was available we placed the split

age

at the mid distance between the parental and the daughter

node ages. This procedure minimizes variance in branch length (Webb et al., 2008). Reconstructed node ages were calculated with the bladj algorithm in Phylocom (Webb et al., 2008). Our modified tree includes 4004 species, 746 of which are insular endemics and 217 of which are extinct (Appendix S1). In most analyses we used all resolved nodes subtending a sister-clade pair, where one clade includes only insular endemics and its sister clade includes only mainland species. We contrasted body size ranges (defined as the difference between the log- transformed masses of the largest and smallest species in a clade) of clade pairs, effectively restricting our analyses to sister taxa. There are 172 such clade pairs, containing in total 1143 species (Appendices S2 & S3). Where the tree contained both insular and mainland species in polytomies under a single node, we arbitrarily defined the insular and mainland species as sister clades, and the parental node as a clade pair. We then repeated the analyses excluding the polytomous clade pairs (see below).

Tests for evolution toward the optimal size

We

used the Fisher exact test to compare the frequency in which

the

median mass within the insular clade is closer to the 100 g

optimum than that of their mainland sister clade, with a null

expected probability of a 1 : 1 ratio. We repeated this test using only fully resolved clades. We further tested for the existence of other possible size optima serving as evolutionary attractors by comparing the fre- quency of insular dwarfism and gigantism in mammals of dif- ferent sizes. We tested whether the median mass of species in insular clades is greater or smaller than the median masses of species in their sister clades for mainland median masses of < 10 g, 10–100 g, 100–1000 g, 1–10 kg and > 10 kg. This test also allowed us to infer whether there is a stronger support for an optimum at 100 g (Brown et al., 1993) or at 1 kg (Damuth, 1993), because, where the masses in the mainland sister clades

are

100–1000 g, the former predicts insular dwarfism whereas

the

latter predicts gigantism. If, however, there are clade-specific

tendencies towards dwarfism or gigantism but no optimal size (Foster, 1964; Meiri et al., 2008), we would expect dwarfism and gigantism to be independent of any optimum.

P. Raia et al.

Tests for decreased size range in insular clades

We defined body size range as the difference in log body mass between the largest and the smallest species within each clade (equal to the largest size ratio in the clade). Under the OST the insular clade is predicted to have a narrower size range than its mainland sister clade.We used three tests of this prediction. First we performed an analysis of covariance (ANCOVA) on the body size ranges of sister clades, with the number of species in a clade as a covariate and insularity (i.e. whether a clade is insular or not) as the main effect. In a second test we simulated body size evolution 1000 times across the whole phylogeny by using the function evolve.phylo in the R library ape (Paradis et al., 2004). From each simulation we drew a body size for each species, computed size ranges of ‘main- land’ and‘insular’ species and calculated the size range difference as insular minus mainland size range. We standardized this dif- ference by dividing it by the simulated mean body size of the mainland clade.This is an index of difference in relative size range between insular and mainland sister clades. The same index was then computed with real data, and compared with the 95% confidence limits computed across all the simulations. Finally, we examined insular size ranges which did not involve clade pairs, while still accounting for taxonomy: we asked whether endemics have narrower size ranges than a random draw of a similar number of species from their family, using only families with at least 10 insular endemics. We produced 999 null samples by picking species at random, without replacement, from the family the insular endemics belong to. We calculated body size ranges for each randomization and assessed significant deviations using two-tailed tests. Body size is phylogenetically conserved within mammalian clades (Freckleton et al., 2002; Blomberg et al., 2003): closely related species tend to have similar sizes. If insular endemics are more closely related than expected by chance (i.e. there is phy- logenetic clustering) testing for size range in these species would produce high type I error, since insular endemics would be expected to be of a similar size whether the OST applies or not. We tested for phylogenetic clustering using two different metrics (Webb, 2000; Webb et al., 2002): the net relatedness index (NRI), which is a standardized measure of the mean phyloge- netic distance (in terms of sum of branch lengths) between a given species and all the other species in the sample averaged over all species in the sample, and the nearest taxon index (NTI), which is a standardized measure of the mean phylogenetic dis- tance between any given species and its sister species, averaged over all species in the sample. Here the ‘sample’ is all insular endemics within a family. Significant NRI and NTI values were estimated via comparison with random distributions produced by drawing n species from the family pool, where n is the number of insular endemics in that family. A total of 999 null samples were produced for significance testing. Other metrics testing for phylogenetic dispersion within samples of species are available, but tend to be highly correlated with each other (Vamosi et al., 2009). Tests for phylogenetic clustering were per- formed in ‘Phylocom’ (Webb et al., 2008).

Table 1 The number of clades in which the median body size in the insular clade is larger (insular gigantism) or smaller (insular dwarfism) than the corresponding value in the mainland sister clade, for mammals of different sizes. Body size classes were assigned according to the median body size in the mainland clades. Probabilities are for deviations from equality in a binomial test. Data are from Appendix S2 in Supporting Information.

Body

Median size smaller on islands

Median size larger on islands

Binomial

size class

probability

< 10 g 10–100 g 100 g–1 kg 1–10 kg > 10 kg

10

13

0.68

31

34

0.80

19

15

0.61

14

13

1

19

1

< 0.0001

RESULTS

Tests for evolution toward the optimal size

In 95 out of 170 cases (55.8%, two pairs with identical island and mainland median masses were excluded) the median body size within the insular clade is closer to 100 g (P = 0.328, two-tailed test). Although many of the polytomies in our dataset are prob- ably hard polytomies (originating from multiple island coloni- zation by a single parental mainland species), we repeated the

test with only fully resolved clades. In this test the median size of the insular clade is closer to 100 g in 42 out of 82 cases (51.2%, P = 0.999). Hence, the 100 g body size does not act as an evolu- tionary attractor for body size of insular taxa. The frequencies of insular dwarfs and giants were similar in all size classes except for the largest one (Table 1). In the largest size class, the median body size of insular species is lower than the median size in their mainland sister clades in all but one clade pair (the mysterious Falkland Island wolf, Dusicyon aus- tralis is larger than its extinct mainland congener Dusicyon a- vus). Thus there is a significant (P < 0.001) tendency for large

( > 10 kg) species to dwarf on islands but to no net trend towards gigantism in small species, and no identified optimal size.

Tests for decreased size range in insular clades

Forty-three clade pairs include more than one species per clade (Table 2). The insular one has a narrower size range in 22. The size ranges of the insular clades is not narrower than that of their mainland sister clades (Wilcoxon paired test, z = - 0.330, P = 0.742). An ANCOVA indicates that size ranges differ between clades (whole model F 2,83 = 24.7, P < 0.001, R 2 = 0.373) but this is due to species richness ( t = 7.02, P < 0.001). The effect of insularity is insignificant (t = 0.60, P = 0.55). Similar results were obtained when we used the clade pair that each size range refers to as a factor (species richness: F = 93.98, P < 0.0001; clade: F = 2.81, P = 0.0006; insularity: F = 0.68, P = 0.41). We further regressed the mainland minus island size-range difference

Table 2 Summary distribution of the occurrence of smaller size range and number of species for clades within a pair. The total number of occurrences per category is reported at the bottom. Only clade pairs including at least two species per clade are included. Nodes correspond to those in Appendix S2 in Supporting Information.

No optimal body size in mammals

Clade pair

Smaller size range on

No. of species larger on

Apodemus argenteus group Antechinus Axis Boromys/Clyomys Cervus Chimarrogale Choloepodini Crocidura Galidiinae

Mainland Mainland Island Mainland Island Island Mainland Island Island Island Mainland Island Mainland Mainland Mainland Mainland Island Mainland Island Mainland Mainland Island Island Island Mainland Mainland Island Island Mainland Island Same Mainland Island Mainland Island Island Island Island Island Mainland Mainland Mainland Island Smaller body size range

Mainland Mainland Same Island Mainland Mainland Island Mainland Mainland Mainland Same Mainland Island Island Island Island Same Island Same Mainland Same Mainland Same Mainland Island Mainland Mainland Mainland Same Mainland Island Same Mainland Island Mainland Same Mainland Island Same Island Mainland Island Island Lower number of species

Hylopetes2

Hystrix Kerivoula argentata group Lemurs/galagos Lutra lutra group Macaca 1 Maxomys Melogale Melomys Microtus arvalis group Monophyllus/Glossophaga Mus 1 Mus 2 Mydaus Naemorhedus Natalus Neotoma albigula group Niviventer Peromyscus Petinomys Phaulomys Presbytis Rattus rattus group Rhinolophus Rousettus Sorex hydrodromus group Stenodermatinae Suncus Sundasciurus Sus Tenrecidae Trichosurini Tupaia Uromys Totals Islands Mainland Same

22

14

20

19

1

10

against the mainland minus island species-richness difference. We contend that a positive intercept indicates that insular size ranges are narrower unless the island clade has more species than the mainland one. This, however, was not the case: the intercept is near zero [0.073, 95% confidence interval (CI):

- 0.056 to +0.201, slope = - 0.28, P < 0.001]. Hence, our tests

demonstrate that body size ranges within clades are a function of clade richness, but not of whether or not it is insular.

Insular clades within clade pairs do not show narrower size ranges than expected in Brownian motion model simulations. Although size ranges of insular clades were narrower than Brownian motion predictions in 14 out of 43 clades (Table 3), in 15 cases the size ranges of the insular clade were wider than expected, again with no apparent phylogenetic bias, for they include bats, rodents, primates, afrosoricids, xenarthrans, dasyurids and diprotodonts.

P. Raia et al.

Table 3 Comparison of actual size ranges differences within a clade pair with data simulated under a Brownian motion (BM) model of evolution.

 

Insular clade

Mainland clade

Mean body size of the mainland clade

Standardized size

Confidence intervals for standardized size ranges according to BM model

Clade pair

size range

size range

difference

Apodemus argenteus group Antechinus Axis Boromys/Clyomys Cervus Chimarrogale Choloepodini Crocidura Galidiinae

0.340

0.311

1.502

0.019

-0.095 to 0.073 -0.089 to 0.056* -0.065 to 0.066 -0.022 to 0.099* -0.098 to 0.042 -0.127 to 0.091† -0.05 to 0.071* -0.105 to 0.034† -0.189 to 0.007† -0.095 to 0.043 -0.086 to 0.087* -0.123 to 0.013† -0.049 to 0.226* -0.015 to 0.066 -0.009 to 0.088* -0.065 to 0.147 -0.073 to 0.081† -0.036 to 0.142* -0.052 to 0.05 -0.089 to 0.032* -0.082 to 0.085* -0.999 to 0.926 -0.055 to 0.055 -0.069 to 0.016† -0.063 to 0.126* -0.101 to 0.033* -0.182 to 0.032 -0.198 to 0.027† -0.073 to 0.076 -0.137 to 0.017† -0.001 to 0.095 -0.058 to 0.053* -0.078 to 0.01† -0.021 to 0.039* -0.178 to 0.002† -0.073 to 0.058 -0.123 to 0.043† -0.049 to 0.16† -0.079 to 0.082† 0.027 to 0.344* -0.121 to 0.038* -0.066 to 0.194 -0.046 to 0.099†

0.830

0.440

1.706

0.229

0.130

0.310

4.695

-0.038

1.050

0.820

1.890

0.122

0.433

0.620

5.060

-0.037

0.019

0.328

1.574

-0.196

0.455

0.070

3.745

0.103

1.213

1.630

1.034

-0.403

0.410

1.420

3.163

-0.319

Hylopetes2

0.760

0.780

2.443

-0.008

Hystrix Kerivoula argentata group Lemurs/galagos Lutra lutra group Macaca 1 Maxomys Melogale Melomys Microtus arvalis group Monophyllus/Glossophaga Mus 1 Mus 2 Mydaus Naemorhedus Natalus Neotoma albigula group Niviventer Peromyscus Petinomys Phaulomys Presbytis Rattus rattus group Rhinolophus Rousettus Sorex hydrodromus group Stenodermatinae Suncus Sundasciurus Sus Tenrecidae Trichosurini Tupaia Uromys

0.920

0.400

4.135

0.126

0.060

0.694

0.662

-0.958

3.670

1.390

2.490

0.916

0.499

0.300

3.890

0.051

0.540

0.130

3.745

0.109

0.555

0.430

2.045

0.061

0.001

0.260

3.100

-0.084

0.650

0.160

1.895

0.259

0.038

0.100

1.500

- 0.041

0.230

0.170

0.993

0.060

0.148

0.030

1.375

0.086

0.085

0.380

1.169

-0.252

0.170

0.310

3.955

-0.035

0.080

0.510

4.565

-0.094

0.440

0.020

0.750

0.560

0.310

0.210

2.293

0.044

0.190

0.438

1.925

-0.129

0.003

0.740

1.516

-0.486

1.350

1.270

2.055

0.039

0.060

0.440

1.475

-0.258

0.050

0.050

3.825

0.000

0.558

0.392

2.145

0.077

0.380

0.860

1.027

-0.467

0.320

0.090

1.945

0.118

0.000

0.830

0.705

-1.177

0.270

0.320

1.205

-0.041

0.934

1.764

0.880

-0.943

0.690

0.820

2.177

-0.060

0.400

1.180

4.650

-0.168

1.940

0.980

2.217

0.433

1.301

0.700

3.417

0.176

0.670

0.450

2.117

0.104

0.380

0.520

2.550

-0.055

*Wider than expected. †Narrower than expected.

Using randomizations, the body size range of insular endemic clades species is not narrower than expected by chance in any of the 16 families with at least 10 species of insular endemics (Table 4). In one family (Tupaiidae) the insular endemics have a wider body size range than expected by chance. These results strongly argue against the prediction

of OST that size ranges in insular taxa are narrow. This is espe- cially striking because insular endemics are phylogenetically clustered (i.e. they are more closely related than expected by chance given the family they belong to, Table 4). Among the 16 families, 11 show phylogenetic clustering (two-tailed tests). Insularity is therefore clearly phylogenetically conservative

No optimal body size in mammals

Table 4 Patterns of phylogenetic dispersion in the occurrence of taxa on islands and their size ranges within mammal families with at least 10 insular endemic taxa.

 

No. of insular species

 

Phylogenetic

Randomized size range ( SD)

Pattern in body size range

P (body size range is random)

Family

NRI

NTI

pattern

Size range

Cercopithecidae

17

7.04***

3.16** Clustering

0.61

0.78 0.19 1.96 1.72 2.44 0.84 3.37 1.64 1.83 0.28 2.43 0.16 2.16 0.84 2.4 1.45 1.01 0.32 1.83 0.05 1.00 0.22 2.27 0.26 1.33 0.25 1.35 0.60 1.52 0.85 1.03 0.26

Random

0.30

Cervidae

10

2.40*

-0.07

Clustering

4.90

Random

0.38

Dasyuridae

11

3.55**

1.88*

Clustering

1.63

Random

0.41

Macropodidae

15

2.66*

2.31*

Clustering

1.61

Random

0.47

Megalonychidae 10

2.43*

2.53***

Clustering

1.40

Random

0.14

Muridae

217

16.97***

4.23***

Clustering

2.29

Random

0.37

Mustelidae

11

3.08*

2.32*

Clustering

1.59

Random

0.32

Phalangeridae

11

1.73

0.18

Random

1.30

Random

0.70

Phyllostomidae

13

2.70*

4.35***

Clustering

0.76

Random

0.37

Pteropodidae

93

3.52**

0.35

Clustering

1.85

Random

0.98

Rhinolophidae

18

-1.26

-1.32

Random

0.94

Random

0.80

Sciuridae

43

5.92*** -2.88** Clustering

2.03

Random

0.38

Soricidae

33

0.97

1.64*

Random

1.31

Random

0.87

Talpidae

10

2.31*

2.47** Clustering

2.11

Random

0.36

Tupaiidae

11

0.73

-1.07

Random

2.45

Larger than expected < 0.05

Vespertilionidae

17

-0.16

0.12

Random

0.92

Random

0.93

*Marginally significant, 0.1 > P > 0.05. **P < 0.05. ***P < 0.01. NRI, net relatedness index; NTI, nearest taxon index.

within mammalian families, but size ranges are not narrow.

DISCUSSION

We find no evidence to support the notion of a single optimal size for mammals. Sizes of members of insular clades were not closer to the putative optima than those of members of their mainland sister clades. Nor was there any evidence to suggest that body size ranges within insular clades are narrower than size ranges in their mainland sister clades, or compared to the pre- dicted differences in size range drawn from simulations per- formed under the Brownian motion model of evolution. Previous studies failed to find evolutionary size attractors despite assuming that competitive size displacement was not a factor in the evolution of the lineages under scrutiny (Alroy, 1998; Roy et al., 2000). Many insular faunas are species poor; hence islands are often viewed as the ideal places for evolution toward the optimal size (Maiorana, 1990; Brown et al., 1993; Damuth, 1993; Lomolino, 2005). Brown et al. (1993) explicitly stated that OST explains the island rule, since insular species can evolve toward the optimal size (100 g) given the reduced com- petition regime they encounter. Here we found no support for the prediction that body sizes of insular taxa are closer to 100 g than are the sizes of allied mainland taxa. We identified strong evidence for dwarfism in large insular mammals, as predicted by the island rule, but our results indicate that this dwarfism only occurs in very large (> 10 kg) mammals, whereas OST predicts dwarfism would start at a much smaller size. Furthermore, we found no evidence for a net trend toward gigantism in small

mammals, which is predicted under both the island rule and OST. Dwarfism above 10 kg, however, seems to be a general mammalian pattern, as the 19 clades showing dwarfism belong to seven orders spanning the entire mammalian phylogeny (diprotodont marsupials, xenarthrans, proboscideans, rodents, carnivores, primates and artiodactyls – although for carnivores we have one case of dwarfism and one of gigantism). Because it posits that small animals evolve larger sizes on islands whereas large animals dwarf, the island rule will, inevi- tably, be associated with some intermediate size at which neither dwarfism nor gigantism is predicted. Our finding, that large mammals dwarf, but small mammals do not, as a rule, grow larger on islands, means that we identify a large size range (all mammals under 10 kg, some 90% of all species in our dataset) where no size evolution is predicted, rather than a unique size value (e.g. 100 g). Thus only very large sizes may be considered ‘suboptimal’ on islands, and a four orders of magnitude size range in which animals will show neither dwarfism nor gigan- tism is at odds with both the island rule and with optimal size theory. Body size ranges are not narrower than expected on islands, and this result persists when we compare actual clade size ranges, compare real size ranges within clades with simulated data, or use the entire phylogeny randomizing the status of insular endemics within families. Given that we find that insular endemics are more phylogenetically closely related to one another than expected by chance, the randomizations within families are very liberal, but we could still not reject the null hypothesis. This may hint that insular clades may have wider distributions than expected, suggesting that insular clades may

P. Raia et al.

fill the entire morphological space despite often being less species rich, in line with the observation that wide size ranges can form even when species richness is low (Brown & Nicoletto, 1991; Cardillo, 2002; Meiri & Thomas, 2007). More tests are needed to resolve this issue. We contend, however, that the eco- logical attributes and particular environment of different insular species probably play a large role in determining body size evo- lution above and beyond phylogenetic effects (Diniz-filho et al., 2009) and possible selection for any optima (Brown et al., 1993; Lomolino, 2005). For species originating through insular radiations, a conflict- ing scenario may be envisioned. An adaptive radiation produces a large number of new species, which may enhance the intensity of interspecific competition, enhancing body size differences between species through character displacement, creating an overall wider body size range (Schluter, 2000; Davies et al., 2007). Thus with an in situ radiation, insular clades may be predicted to have larger ranges than expected by chance. Of the insular clades we analysed (Tables 1 & 2), insular radiations can be invoked for Madagascar’s tenrecs and lemurs, and perhaps for Indonesian mosaic-tailed rats (genus Melomys), Maxomys mice, Hystrix porcupines and bare-backed fruit bats (genus Dobsonia); for New Guinean dasyures (genera Antechinus and Murexia); and for Antillean cave rats (genera Boromys, Botromys and Heteropsomys ). The vast majority of insular clades, however, do not represent such radiations, and even the Indonesian and Antilles examples we cite above correspond to insular endemics inhabiting different islands within an archipelago, that probably evolved in isolation. Thus, there is no convincing evidence that in situ speciation and ensuing competition on islands may have driven species away from the optimal body size. Our results are at odds with the idea of multiple, large-clade- specific body size optima on islands (Lomolino, 2005). We found no support for the prediction that insular faunas evolve smaller size ranges on islands, a prediction that is independent of the optimal value per se . Lomolino (2005) referred mainly to mammalian orders when suggesting multiple, body-plan- specific optima and thus our family-level analyses should have been able to detect them. Thus, we doubt the existence of size optima in general, whatever these optimal values actually are, or to which phylogenetic or taxonomic level they are thought to relate. We argue that the island rule, whether it is true or an epiphe- nomenon of the tendency of some clades to evolve either large or small body sizes on islands (Lawlor, 1982; Meiri et al., 2008), is better studied by considering contingent factors such as species biology and the ecological characteristics of island faunas (Lawlor, 1982; Raia et al., 2003; Raia & Meiri, 2006). These cannot be captured by one set of allometric equations, resulting in a ‘one size fits all’ theory such as the OST. We find that OST is an unlikely explanation for the evolution of body size on islands. Similarly, we found no support for the idea that there is an evolutionary attractor for mammal species evolving on islands. The theoretical basis of OST is outside the scope of our dis- cussion, yet it is remarkable that this theory fails to apply

under the circumstances which best match its predictions (on islands). We conclude that, while dwarfism in large mammals is a real net trend, gigantism in small mammals is more idio- syncratic. The evolution of clade-specific size ranges is inde- pendent of insularity.

ACKNOWLEDGEMENTS

We thank Ally Phillimore for insightful discussion leading to the start of this project. We thank Joaquin Hortal and Mark Lomolino for valuable discussion. Anna Loy, David Currie, José Alexandre Diniz-Filho and three anonymous referees kindly pro- vided important comments on this manuscript. Tassos Kotsakis and FedericaMarcolini gave us unpublished data and shared with us their opinion about the systematic position of some insular rodents they are studying. Felisa Smith kindly provided us with a new version of her mammalian body size database.

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P. Raia et al.

BIOSKETCHES

Pasquale Raia is a post-doctoral research fellow at the Department of Earth Science, University of Naples Federico II, and a member of the Center for Evolutionary Ecology based at Rome III University. He is interested in large mammal evolution, both at the organismal and community levels, in response to climate change and to the effect of ecological interactions.

Francesco Carotenuto is a post-doctoral research fellow at the Department of Earth Science University of Naples. His research interests focus on Quaternary mammal macroecology and biogeography.

Shai Meiri is a senior lecturer at the Department of Zoology, Tel Aviv University. He is interested in trait evolution, the tempo and mode of evolution, the evolutionary implications of biogeography, vertebrate evolution and large wooden badgers.

Editor: José Alexandre F. Diniz-Filho

SUPPORTING INFORMATION

Additional Supporting Information may be found in the online version of this article:

Appendix S1 Phylogenetic tree used for this study, along with extinct species included, their body size and source papers used to ascertain both their size and phylogenetic position. Appendix S2 Clade pairs partitioned in mainland and insular daughter clades. Appendix S3 Species belonging to clade pairs.

As a service to our authors and readers, this journal provides supporting information supplied by the authors. Such materials are peer-reviewed and may be reorganized for online delivery, but are not copy-edited or typeset. Technical support issues arising from supporting information (other than missing files) should be addressed to the authors.

APPENDIX S1

A. Extinct species included in this study

B. References for size estimates and phylogenetic affinities for extinct species

C. Phylogeny of all 4004 species used in the study

A. Extinct species included in the phylogenetic tree used for this study.

For each species we report whether or not it was an insular endemic, its log 10 body mass (in grams), and the sources used to get body mass and phylogenetic data. Where the same source provided both size and phylogenetic data, the last column was left empty.

Species

insularity

log

body mass reference

Phylogeny reference

 

mass

Capromeryx minor

no

4.32

Brook & Bowman 2004

Janis & Manning

 

1998

Stockoceros conklingi

no

4.72

Brook & Bowman 2004

Janis & Manning

 

1998

Tetrameryx shuleri

no

4.79

Brook & Bowman 2004

Janis & Manning

 

1998

Capromeryx mexicana

no

4.18

Smith et al. 2003

Janis & Manning

 

1998

Stockoceros onusrosagris

no

4.74

Smith et al. 2003

Janis & Manning

 

1998

Bison antiquus

no

6.01

Brook & Bowman 2004

Geraards 1992

Bison latifrons

no

6.02

Brook & Bowman 2004

Geraards 1992

Bos primigenius

no

5.97

Meloro et al., 2007

Geraards 1992

Bison priscus

no

5.95

Smith et al. 2003

Geraards 1992

Pelorovis antiquus

no

6

Smith et al. 2003

Geraards 1992

Bootherium bombifrons

no

5.88

Brook & Bowman 2004

McDonald & Ray

 

1989

Euceratherium collinum

no

5.7

Brook & Bowman 2004

McDonald & Ray

 

1989

Symbos cavifrons

no

5.6

Smith et al. 2003

McDonald & Ray

 

1989

Megalotragus priscus

no

5.3

Smith et al. 2003

Vrba 1979

Antidorcas australis

no

4.6

Smith et al. 2003

placed with A. marsupialis

Antidorcas bondi

no

4.53

Smith et al. 2003

placed with A. marsupialis

Species

insularity

log

body mass reference

Phylogeny reference

 

mass

Oreamnos harringtoni

no

4.88

Smith et al. 2003

placed with O. americanus

Camelus thomasi

no

5.7

Smith et al. 2003

Feranec 2003

Hemiauchenia macrocephala

no

5.04

Smith et al. 2003

Feranec 2003

Hemiauchenia paradoxa

no

6

Smith et al. 2003

Feranec 2003

Palaeolama mirifica

no

4.9

Smith et al. 2003

Feranec 2003

Dusicyon australis

yes

4.699

Brook & Bowman 2004

Zrzavy & Rikankova

 

2003

Dusicyon avus

no

4.11

Smith et al. 2003

Zrzavy & Rikankova

 

2003

Isolobodon portoricensis

yes

3.1

Nowak 1999, It is a conservative estimate as this species was probably larger than P. aedium

Woods et al. 2001

Plagiodontia ipnaeum

yes

3.1

Nowak 1999, It is a conservative estimate as this species was probably larger than P. aedium

Woods et al. 2001

Hexolobodon phenax

yes

3.75

Nowak 1999, It is suggested it was the size of Capromys pilorides

Woods et al. 2001

Isolobodon montanus

yes

3.1

Nowak 1999, reportedly Isolobodon was the same size of Plagiodontia

Woods et al. 2001

Castoroides ohioensis

no

5.18

Smith et al. 2003

placed sister to C. fiber

Praemegaceros cretensis

yes

4.9

based on size ratio as reported in Raia & Meiri 2006

Croitor 2004, Raia & Meiri 2006

Praemegaceros ropalophorus

yes

4.476

based on size ratio as reported in Raia & Meiri 2006

Croitor 2004, Raia & Meiri 2006

Praemegaceros cazioti

yes

4.845

estimate from Burness et al. 2001

Croitor 2004, Raia & Meiri 2006

Megaloceros giganteus

no

5.59

Meloro et al., 2007

Lister et al. 2005

Cervus astylodon

yes

4.267

Matsumoto & Otsuka 2000; Based on the cubic ratio of radius length as compared to Cervus nippon multiplied by the size of the latter. The morhotype used for comparison is G4 , which is the stratigraphically youngest.

Species

insularity

log

body mass reference

Phylogeny reference

 

mass

Cervalces scotti

no

5.8

Smith et al. 2003

placed sister to Alces

Sinomegaceros yabei

yes

5.589

van der Made & Tong 2008 state S. yabei is large, possibly as large as M. giganteus

Dasypus bellus

no

4.65

Smith et al. 2003

Gaudin 2003,

 

Vizcaino 2009

Holmesina septentrionalis

no

5.4

Smith et al. 2003

Gaudin 2003,

 

Vizcaino 2009

Holmesina occidentalis

no

5.3

Smith et al. 2003

Gaudin 2003,

 

Vizcaino 2009

Holmesina paulacoutoi

no

5.1

Smith et al. 2003

Gaudin 2003,

 

Vizcaino 2009

Pampatherium humboldtii

no

5.18

Smith et al. 2003

Gaudin 2003,

 

Vizcaino 2009

Pampatherium typum

no

5.3

Smith et al. 2003

Gaudin 2003,

 

Vizcaino 2009

Kraglievichia paranense

no

4.653

Brook & Bowman 2004

Gaudin 2003,

 

Vizcaino 2009

Sarcophilus laniarius

no

4.08

Smith et al. 2003

placed sister to S. harrisi

Daubentonia robusta

yes

4.7

Brook & Bowman 2004

name given to fossil remains of D. madagascarensis according to Wilson & Reeder (2003)

Diprotodon minor

no

5.95

Smith et al. 2003

Black 2008

Diprotodon optatum

no

6.18

Smith et al. 2003

Black 2008

Euryzygoma dunese

no

5.7

Smith et al. 2003

Black 2008

Hulitherium thomasettii

yes

5.14

Smith et al. 2003

Black 2008

Kolopsis watutense

yes

5.48

Smith et al. 2003

Black 2008

Maokopia ronaldi

yes

5

Smith et al. 2003

Black 2008

Nototherium mitchelli

no

5.7

Smith et al. 2003

Black 2008

Zygomaturus trilobus

no

5.88

Smith et al. 2003

Black 2008

Boromys offella

yes

2.61

Turvey et al. 2007

Woods et al. 2001

Boromys torrei

yes

2.29

Turvey et al. 2007

Woods et al. 2001

Brotomys voratus

yes

2.86

Turvey et al. 2007

Woods et al. 2001

Heteropsomys insulans

yes

3.34

Turvey et al. 2007

Woods et al. 2001

Elephas namadicus

no

6.81

After measurements in Maglio (1973) it is apparent E.antiquus &

Thomas et al. 2000, Maglio 1973, Shoshani & Tassy

 

E.namadicus were the same body size

2005

Species

insularity

log

body mass reference

Phylogeny reference

 

mass

Elephas creutzburgi

yes

6.57

based on size ratio as reported in Raia & Meiri 2006

Thomas et al. 2000, Maglio 1973, Shoshani & Tassy

 

2005

Elephas cypriotes

yes

5.482

based on size ratio as reported in Raia & Meiri 2006

Thomas et al. 2000, Maglio 1973, Shoshani & Tassy

 

2005

Elephas mnaidriensis

yes

6.272

based on size ratio as reported in Raia & Meiri 2006

Thomas et al. 2000, Maglio 1973, Shoshani & Tassy

 

2005

Mammuthus lamarmorae

yes

5.812

based on size ratio as reported in Raia & Meiri 2006

Thomas et al. 2000, Maglio 1973, Shoshani & Tassy

 

2005

Palaeoloxodon naumanni

yes

6.348

estimated by using

Thomas et al. 2000,

 

regression equations in Roth (1990) & average

Maglio 1973, Shoshani & Tassy

shoulder height of 225 cm reported in Kondo et al. 2001

2005

Elephas antiquus

no

6.81

Meloro et al., 2007

Thomas et al. 2000, Maglio 1973, Shoshani & Tassy

 

2005

Mammuthus columbi

no

6.9

Smith et al. 2003

Thomas et al. 2000, Maglio 1973, Shoshani & Tassy

 

2005

Mammuthus imperator

no

7

Smith et al. 2003

Thomas et al. 2000,

 

Maglio 1973,

Shoshani & Tassy

2005

Mammuthus primigenius

no

6.74

Smith et al. 2003

Thomas et al. 2000, Maglio 1973, Shoshani & Tassy

 

2005

Mammuthus exilis

yes

5.23

the cubed ratio of M.e.

Thomas et al. 2000,

 

to Elephas falconeri's

Maglio 1973,

long bones multiplied

Shoshani & Tassy

by the estimated size of E.f.

2005

Onohippidium sp

no

5.49

Stromberg 2006

Stromberg 2006

Equus hydruntinus

no

5.32

Meloro et al., 2007

Burke et al. 2003

Hippidion principale

no

5.71

Smith et al. 2003

Stromberg 2006

Hippidion saldiasi

no

5.42

Smith et al. 2003

Stromberg 2006

Homotherium serum

no

5.43

Brook & Bowman 2004

Slater & Van Valkenburgh 2004

Species

insularity

log

body mass reference

Phylogeny reference

 

mass

Panthera atrox

no

5.63

Brook & Bowman 2004

Slater & Van Valkenburgh 2005

Miracinonyx trumani

no

4.94

Smith et al. 2003

Slater & Van Valkenburgh 2006

Smilodon fatalis

no

5.64

Smith et al. 2003

Slater & Van Valkenburgh 2007

Smilodon populator

no

5.65

Smith et al. 2003

Slater & Van Valkenburgh 2007

Giraffa gracilis

no

5.93

Smith et al. 2003

placed sister to G. camaleopardalis

Chlamydotherium spp.

no

5.24

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Glyptodon clavipes

no

6.3

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Glyptodon reticulatus

no

5.94

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Glyptotherium floridanum

no

6.04

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Glyptotherium mexicanum

no

6.04

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Lomaphorus spp.

no

5.4

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Neosclerocalyptus spp.

no

5.3

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Neothoracophorus depressus

no

6.04

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Neothoracophorus elevatus

no

5.9

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Panochthus tuberculatus

no

6.03

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Plaxhaplous canaliculatus

no

6.11

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Species

insularity

log

body mass reference

Phylogeny reference

 

mass

Sclerocalyptus ornatus

no

5.45

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Doedicurus clavicaudatus

no

6.17

Smith et al. 2003

Gaudin 2003, Gaudin & Wible 2006, Vizcaino 2009

Cuvieronius hyodon

no

6.623

Brook & Bowman 2004

Shoshani & Tassy

 

2005

Cuvieronius spp.

no

6.7

Smith et al. 2003

Shoshani & Tassy

 

2005

Haplomastodon chimborazi

no

6.78

Smith et al. 2003

Shoshani & Tassy

 

2005

Notiomastodon spp.

no

6.79

Smith et al. 2003

Shoshani & Tassy

 

2005

Stegomastodon superbus

no

6.88

Smith et al. 2003

Shoshani & Tassy

 

2005

Amblyrhiza inundata

yes

4.97

McFarlane et al. 1998

Flemming &

 

MacPhee 1996

Quemisia gravis

yes

4.14

Nowak 1999, reportedly

Flemming &

 

the same size of Elasmodontomys

MacPhee 1996

Clidomys osborni

yes

4.66

Nowak 1999. Weight

Flemming &

 

estimate obtained as the cubic ratio of this species to C. pyloroides body size, the latter taken 5650 grams &

MacPhee 1996

450

mm in head-body

length

Clidomys parvus

yes

4.36

Nowak 1999. Weight

Flemming &

 

estimate obtained as the cubic ratio of this species to C. pyloroides body size, the latter taken 5650 grams &

MacPhee 1996

450

mm in head-body

length

Elasmodontomys obliquus

yes

4.14

Smith et al. 2003

Flemming &

 

MacPhee 1996

 

yes

5.7

Brook & Bowman 2004

Boisserie 2005

Hippopotamus madagascariensis Hippopotamus lemerlei

yes

5.699

MOM-Mammals Version 3.61 (current as of January 2007)

Boisserie 2005

Hippopotamus creutzburgi

yes

5.741

Raia & Meiri 2006

Boisserie 2005

Hippopotamus pentlandi

yes

6.182

Raia & Meiri 2006

Boisserie 2005

Species

insularity

log

body mass reference

Phylogeny reference

 

mass

Hippopotamus laloumena

yes

5.98

Smith et al. 2003

Boisserie 2005

Neochoerus aesopi

no

4.79

Prevosti & Vizcaíno

Prado et al. 1998

 

2006

Neochoerus pinckneyi

no

4.85

Smith et al. 2003

Prado et al. 1998

Neochoerus sulcidens

no

5.18

Smith et al. 2003

Prado et al. 1998

Archeolemur edwardsi

yes

4.34

Brook & Bowman 2004

Orlando et al. 2008

Archeolemur majori

yes

4.23

Brook & Bowman 2004

Orlando et al. 2008

Hadropithecus stenognathus

yes

4.45

Brook & Bowman 2004

Orlando et al. 2008

Mesopropithecus dolichobrachion

yes

4.08

Brook & Bowman 2004

Orlando et al. 2008

Mesopropithecus globiceps

yes

4

Brook & Bowman 2004

Orlando et al. 2008

Mesopropithecus pithecoides

yes

4.04

Brook & Bowman 2004

Orlando et al. 2008