Journal of Biogeography (J. Biogeogr.) (2011) 38, 89–100

ORIGINAL Slaying dragons: limited evidence for ARTICLE unusual body size evolution on islands Shai Meiri1*, Pasquale Raia2 and Albert B. Phillimore3

1Department of Zoology, Faculty of Life ABSTRACT Sciences, Tel Aviv University, 69978 Tel Aviv, Aim Island taxa often attain forms outside the range achieved by mainland Israel, 2Dipartimento di Scienze della Terra, Universita` Federico II, 80138 Naples, Italy, relatives. Body size evolution of vertebrates on islands has therefore received 3Division of Biology, Imperial College at much attention, with two seemingly conflicting patterns thought to prevail: (1) Silwood Park, Ascot SL5 7PY, UK islands harbour animals of extreme size, and (2) islands promote evolution towards medium body size (‘the island rule’). We test both hypotheses using body size distributions of mammal, lizard and bird species. Location World-wide. Methods We assembled body size and insularity datasets for the world’s lizards, birds and mammals. We compared the frequencies with which the largest or smallest member of a group is insular with the frequencies expected if insularity is randomly assigned within groups. We tested whether size extremes on islands considered across mammalian phylogeny depart from a null expectation under a Brownian motion model. We tested the island rule by comparing insular and mainland members of (1) a taxonomic level and (2) mammalian sister species, to determine if large insular animals tend to evolve smaller body sizes while small ones evolve larger sizes. Results The smallest species in a taxon (order, family or genus) are insular no more often than would be expected by chance in all groups. The largest species within lizard families and bird genera (but no other taxonomic levels) are insular more often than expected. The incidence of extreme sizes in insular mammals never departs from the null, except among extant genera, where gigantism is marginally less common than expected under a Brownian motion null. Mammals follow the island rule at the genus level and when comparing sister species and clades. This appears to be driven mainly by insular dwarfing in large-bodied lineages. A similar pattern in birds is apparent for species within orders. However, lizards follow the converse pattern. Main conclusions The popular misconception that islands have more than their fair share of size extremes may stem from a greater tendency to notice gigantism and dwarfism when they occur on islands. There is compelling evidence for insular dwarfing in large mammals, but not in other taxa, and little evidence for the second component of the island rule – gigantism in small-bodied taxa. *Correspondence: Shai Meiri, Department of Keywords Zoology, Faculty of Life Sciences, Tel Aviv University, 69978 Tel Aviv, Israel. Birds, dwarfism, evolution, gigantism, island biogeography, island rule, lizards, E-mail: [email protected] mammals.

pygmy humans all spring to mind when the body sizes of INTRODUCTION island vertebrates is discussed. Body size evolution on islands is Giant tortoises, enormous flightless birds and huge bears, perceived to be fast (Lister, 1989; Millien, 2006) and has alongside minute deer, tiny lizards, dwarf elephants and, lately, produced extreme phenotypes, with the smallest or the largest

ª 2010 Blackwell Publishing Ltd www.blackwellpublishing.com/jbi 89 doi:10.1111/j.1365-2699.2010.02390.x S. Meiri et al. species of many clades being insular (Hooijer, 1967; Berry, mixed support for this rule (Clegg & Owens, 2002; Boback & 1998; Greer, 2001; Glaw et al., 2006; Whittaker & Ferna´ndez- Guyer, 2003; Lomolino, 2005; Meiri, 2007), with the best Palacios, 2007; Hedges, 2008; Losos & Ricklefs, 2009). For support coming from data for mammals (Lomolino, 1985; example, the St Helena earwig, Labidura herculeana, the Price & Phillimore, 2007; Welch, 2009; but see Meiri et al., Indonesian stick insect, Pharnacia serratipes, and the New 2004, 2006, 2008). Size evolution is often hypothesized to be Zealand giant wetas (Deinacrida spp.) are probably the largest most drastic on small islands, with island area showing representatives of their clades (Chown & Gaston, 2010). complex interactions with body size (Heaney, 1978), but Similarly, the world’s largest bat (Smith et al., 2003) is the empirical patterns are equivocal (e.g. Meiri et al., 2005b; Wu Philippine-endemic golden crowned flying fox, Acerodon et al., 2006; Schillaci et al., 2009). jubatus, the largest Quaternary bird was the Madagascan These two hypotheses, that islands should harbour extreme elephant bird, Aepyornis maximus, and the largest raptor was sizes, and that they should harbour taxa that are closer to a clade- the New Zealand endemic Haast’s eagle, Harpagornis moorei wide mode, need not necessarily be contradictory (Fig. 1). If a (Worthy et al., 2002; Murray & Vickers-Rich, 2004). clade, such as mammals, has a single size attractor (e.g. Brown Among reptiles, the largest living lizard (the Komodo et al., 1993) then members of a subclade may evolve to a size dragon, Varanus komodoensis) and tortoises (the giant tor- extreme: insular members of a subclade of large-bodied animals toises of Aldabra and the Galapagos, Geochelone gigantea and (e.g. elephants) will be the smallest within this subclade, but not Geochelone elephantopus) are insular endemics (Arnold, 1979; across the larger clade as a whole. Similarly, insular members of a Meiri, 2008). Islands also harbour the smallest members of subclade of small-bodied animals (e.g. shrews) may be the largest several clades: the smallest bird is believed to be the Cuban bee members of this subclade, but not the largest mammals overall. hummingbird, Mellisuga helenaei (although Dunning, 2008b, If, however, each subclade has its own optimal size that its insular suggests that Thaumastura cora from mainland Peru is members evolve towards (Lomolino, 2005) then islands should smaller), and species of Caribbean Leptotyphlops and Sphaero- harbour few size extremes (Fig. 1c). dactylus are the world’s smallest snakes and lizards, respectively The seemingly conflicting discussion of insular size extremes (Hedges, 2008; Meiri, 2008). This perceived abundance of on the one hand, and insular medium sizes on the other hand, insular size extremes is usually thought to be a response to the stems in part from the different phylogenetic and temporal scope low intensity of competition and predation both within and of studies dealing with them. Studies of size extremes are usually across taxa: the absence of carnivorous mammals is most often conducted at the inter-specific level (Glaw et al., 2006; Hedges, quoted as allowing the evolution of large size in birds (mainly 2008), and often deal with extinct taxa (Kurten, 1953; Sondaar, through the evolution of flightlessness; e.g. Bunce et al., 2005; 1977; Steadman et al., 2002; Raia et al., 2003). The study of Murray & Vickers-Rich, 2004), reptiles (e.g. Case, 1978; Meiri, evolution towards medium sizes usually involves intra-specific 2008) and small mammals (e.g. Angerbjo¨rn, 1986; Adler & studies of insular and mainland populations of extant species Levins, 1994). Alternatively, this perceived pattern may simply (e.g. Lomolino, 1985; Boback & Guyer, 2003; Meiri, 2007). reflect an ascertainment bias, i.e. we may be more likely to Evolutionary processes above and below the species level notice animals of extreme body size when they happen to live may differ through, for example, species sorting and adaptive on islands (Whittaker & Ferna´ndez-Palacios, 2007). radiation in the former versus inter-island and island– By contrast, the island rule suggests that, rather than showing mainland gene flow in the latter (Jablonski, 2008). As far as size extremes on islands, insular populations should be closer to we are aware McClain et al. (2006) and Welch (2010) present the clade-wide median body size than their mainland counter- the only purely inter-specific studies of the island rule, parts (Lomolino, 1985, 2005). According to the island rule, comparing mean sizes within genera of deep sea (= ‘insular’ populations of small species will evolve larger size, populations in McClain et al.) and shallow sea (‘mainland’) species, rather of large species will dwarf, and populations of average-sized than using comparisons within single species. An argument for species will show little size evolution on islands (Lomolino, 2005; extending tests of the island rule to the species level is that the Welch, 2009). Viewed at the clade level, the island rule predicts selection pressures thought to promote convergence on a stabilizing selection: on islands an individual should not be median body size for island populations should act similarly either too large or too small. Once the optimum is reached (via on island species. The major difference between the two directional selection on the founding population), stabilizing scenarios is that there should be less gene flow between species selection should maintain phenotypes around it. Interestingly, than between populations, meaning that evolution should an opposite pattern of disruptive selection and increased vari- proceed more rapidly in the former. However, there is no ance is often thought to prevail within populations on islands obvious reason why the type of selection and adaptive optima (Van Valen, 1965; Scott et al., 2003; cf. Meiri et al., 2005a). should differ in these two contexts. A major advantage of The island rule is thought to manifest the combined effects intra-specific studies of insular size evolution is that they of lower predation pressures on islands (Heaney, 1978), compare very closely related taxa (i.e. different populations character release in the absence of competitors (Dayan & within a species), usually from areas that are in geographic Simberloff, 1998) and the paucity of resources on islands proximity. Intra-specific comparisons thus control for much of driving dwarfism in large-bodied forms (Lomolino, 2005). the variation in size that is unrelated to insularity. Restricting Empirical evidence from terrestrial vertebrate studies provides ourselves to intra-specific studies, however, we may be missing

90 Journal of Biogeography 38, 89–100 ª 2010 Blackwell Publishing Ltd Island vertebrates and body size extremes

No island rule, no insular size extremes No island rule, insular size extremes Island rule, no insular size extremes

(a) (b) (c) Body size of island taxa

Body size of mainland taxa

Island rule, insular size extremes No island rule, insular size extremes Reversed island rule, insular size extremes

(d) (e) (f) Body size of island taxa

Body size of mainland taxa

Figure 1 Schemes showing possible ways in which patterns of body size on islands and mainland within taxa (size extremes or average sizes) can combine to produce patterns of body size across taxa (slope <1, slope = 1, slope >1). x-axis, mainland body size; y-axis, island body size; dashed line, a line with an intercept of 0 and a slope of 1; solid line, slope returned by standardized major axis regression (can mask the dashed line). The body size frequency distributions depict insular (top) and mainland members of a clade (bottom). The mainland mean size is indicated by the vertical, dashed line. (a) The null distribution. No insular size extremes, no island rule (slope of 1, similar insular and mainland size ranges). (b) There are size extremes because island taxa have wider size distributions, but no island rule because mean sizes are similar (slope of 1). (c) The island rule holds (small animals evolve larger size and large ones dwarf, slope <1), but no size extremes because island taxa have narrower size distributions. (d) The island rule holds (slope <1), and insular clades are of extreme size – members of large-bodied clades are smallest in their clade and members of small-bodied clades are the largest in their clade. (e) Island members are proportionally always larger than mainland ones, hence there is one type of size extreme, but no island rule (no dwarfing of large animals, slope = 1). (f) There are size extremes, but in the opposite direction than predicted under the island rule. Small- sized insular animals are extremely small, large ones are extremely large (slope >1). the more dramatic cases of insular size evolution, where We use nearly complete datasets of species body sizes of changes are drastic enough to merit different specific status. mammals, birds and lizards. For mammals (only) a compre- Thus intra-specific studies will omit from consideration, for hensive species-level phylogeny and an excellent late Pleisto- example, Elephas falconeri, which evolved to just 1% of the cene fossil record exist. This meant that we were also able to mass of its mainland ancestor (Roth, 1992), and even studies use a sister-clade comparison, and include data for species conducted on species within genera will miss members of that went extinct since the end of the last glacial, which insular endemic genera such as the c. 100 kg insular rodent include some of the most pronounced cases of insular size Amblyrhiza inundata (Biknevicius et al., 1993) and the largest evolution. gecko, Hoplodactylus delcourti (Russell & Bauer, 1986). Here we examine, in a purely inter-specific fashion, whether: MATERIALS AND METHODS (1) species with extreme body sizes (i.e. the largest and smallest species) in a subclade are more often insular endemics than Data expected by chance given the number of insular endemics in the subclade; and (2) if there is evidence for a pattern Body size data are species specific. Body size (snout–vent lengths consistent with the island rule above the species level using in mm) and insularity data for lizards (Appendix S1a in the mean sizes of insular and mainland species within clades. Supporting Information) are from an updated version of the

Journal of Biogeography 38, 89–100 91 ª 2010 Blackwell Publishing Ltd S. Meiri et al. dataset of Meiri (2008). Lizard taxonomy follows Uetz et al. Only genera having at least one insular member and one (2009). continental member were included. We repeated this proce- Body mass data (in g) for birds are from Dunning (2008). dure at the family and order levels (family level only for Where mass data were reported for multiple subspecies the mean lizards). of these measurements was taken (intra-specific data were first We then assessed whether the observed values departed from log10-transformed). For each species overall mean body mass the null expectation if insular status were randomly assigned was estimated across means for female, male and unsexed birds. by randomly selecting n individuals per taxon (i.e. genus, We obtained data on avian insularity from McCall (1997), and family or order), where n is the number of insular species in supplemented and verified them using Avibase (http:// that taxon. We then calculated the number of taxa for which avibase.bsc-eoc.org) and regional guides (Appendix S1b). Tax- the largest or smallest representative had been randomly onomy follows Clements (1998), and we included species that assigned insular status. This process was repeated 10,000 times had been extirpated since the extinction of the dodo (17th to obtain a distribution of the null expectation for the century). As we were interested in the effect of insularity on frequency of insular gigantism or dwarfism. We calculated the birds, we excluded birds that forage at sea, which we defined as all proportion of the null distribution that was: (1) greater than or members of the Alcidae, Diomedeidae, Fregatidae, Hydrobat- equal to the observed value, and (2) smaller than or equal to idae, Laridae, Pelecanidae, Pelecanoididae, Phaethontidae, the observed value. The smaller of these proportions was Phalacocoracidae, Procellariidae, Rynchopidae, Spheniscidae, multiplied by 2 to give a two-tailed P-value. Stercoraridae, Sternidae and Sulidae families. Our randomization test for size extremes on islands should Body mass and insularity data for mammals are from the be conservative for two reasons. First, we classify all species 2007 version of Smith et al. (2003) (data kindly provided by that have at least one mainland population as ‘mainland’, Felisa Smith), supplemented with literature data (see Appen- even though in some of these species the largest or smallest dix S1c for species for which we obtained data from sources populations may be insular (e.g. Kodiak brown bears, Ursus other than the Smith et al. database). Mammal insularity was arctos middendorffi). Second, if insular taxa are clustered verified using Wilson & Reeder (2005), regional guides and within a subclade (as is the case in mammals; Raia et al., palaeontological accounts of fossil species. We use only fossil 2010), the variance in body size among insular members of a mammals that went extinct since the end of the last glacial. subclade will be reduced, reducing the potential for the Only fossil species known to be confined to islands during the evolution of size extremes. However, it is possible that the last glacial were considered to be insular. ancestral members of subclades that colonize islands are

All analyses were conducted on log10-transformed measures themselves biased in size with respect to the mainland of body size, to bring the intra-class distribution of body size representatives of the subclade (e.g. they may be very large; closer to a normal distribution and to remove a relationship Lomolino, 1985) and this could generate an increased between the mean and variance of a group (Lynch & Walsh, incidence of insular size extremes without requiring further 1998). evolution on islands. In the absence of adequate fossil data we are unable to test this hypothesis. Using the mammalian phylogeny we were able to compare Phylogeny the observed incidence of size extremes with those generated Complete species-level phylogenetic data exist only for mam- under a phylogenetically explicit null model. We conducted mals, and we thus only use phylogenetic analysis on this group. 1000 simulations of body size evolution across the whole We used the species-level mammal supertree of Bininda- phylogeny following a Brownian motion (random walk with Emonds et al. (2007). The tree was modified as follows: we constant variance) model using the evolve.phylo function in resolved taxonomic discrepancies between the tree and our the R library ‘ape’ (Paradis et al., 2004). A recent study on data using the taxonomy of Wilson & Reeder (2005), and body size evolution across the mammalian tree identified a excluded species for which we had no size data and fossil weak but significant signature of early burst evolution (i.e. species whose island endemism was uncertain. Finally, where decelerating rates of phenotypic evolution; Cooper & Purvis, the phylogenetic affinities of extinct species are well under- 2010). However, a constant-rate Brownian motion model did stood we added them to the tree. Our modified tree includes not perform much worse, and in the context of our study 3961 species. Although this tree excludes some new phyloge- should represent an unbiased means of generating a phyloge- netic data, it is the only comprehensive species-level tree netically explicit null expectation. The fossil record shows that currently available for any vertebrate class. mammals have increased in body size through time according to Cope’s rule (e.g., Alroy, 1998), which conflicts with a Brownian model. Nonetheless, with respect to the hypotheses Statistical analysis being tested here, adding directionality (universally across island and mainland lineages) to a random walk should not Size extremes bias our tests. For each simulation we quantified the incidence For each of the four datasets we counted the number of genera of gigantism and dwarfism and in this manner generated a null for which either the largest or the smallest species was insular. distribution. We then used two-tailed tests to establish the

92 Journal of Biogeography 38, 89–100 ª 2010 Blackwell Publishing Ltd Island vertebrates and body size extremes probability of obtaining the observed incidences of gigantism distribution-free randomization approach of Welch (2009) and dwarfism under the null Brownian model. described above. All statistical analyses were conducted in R (R Development Core Team, 2008) and all tests were two-tailed. Mean size RESULTS We assessed whether the ‘island rule’ applies above the species level. We calculated the mean log body size of insular and 10 Lizards mainland species within each genus. We tested the null hypothesis that there are no differences between patterns of Of 5380 lizards in our dataset, 1636 are insular endemics mainland and insular size evolution across genera (Welch, (Appendix S1a). The largest lizard in 9 of 19 families is an 2009) by examining the slope of the island versus mainland insular endemic (see size frequency histograms in Appen- taxon means using standardized major axis (= reduced major dix S3a), while the median expected number is five (P = 0.07). axis) regression. A slope <1 is expected under the island rule, At the genus level the number of largest insular species is no which predicts gigantism in small-bodied taxa and dwarfism in different from the null expectation. The number of insular large-bodied ones and a reduction of variance amongst insular species that are the smallest species in their genus or family is taxa as compared with their mainland counterparts (Price & likewise not statistically different from that expected by chance Phillimore, 2007). Different taxa within a taxonomic level will (Table 1). vary in age, meaning that the expected variance of phenotypes The SMA slope between the taxon mean masses on islands among them is likely to vary. This heterogeneity of expected versus mainland does not depart significantly from 1 at the variance violates an assumption of standardized major axis genus level (Fig. 2a). At the family level the slope estimate of (SMA) regression. We therefore used a distribution-free 1.24 [95% confidence interval (CI) = 1.02–1.50] (Fig. 2b) is variant of the SMA test, as proposed by Welch (2009). The significantly steeper than 1 using both SMA (r = 0.49, SMA correlation coefficient (r) between x + y (where x is body P < 0.05) and the distribution-free randomization test size on the mainland and y is body size on an island) and x ) y (P < 0.05, similar to the pattern depicted in Fig. 1f). was the test statistic. The observed correlation coefficient was then compared with that observed when the identity of insular Table 1 Actual and expected numbers of taxa in which insular means was randomized with respect to x and y (Welch, 2009). members are the largest or the smallest, in different taxa at dif- Ten thousand randomizations were conducted and the two- ferent taxonomic levels. tailed P-value was the smaller of twice the proportion of randomized correlation coefficients that were either greater Number than or equal to or less than or equal to the observed Clade Level of clades Largest Smallest correlation. If the observed SMA correlation between x + y Lizards Genus 85 30 (36) 36 (35) ) and x y was significantly greater than expected at random Lizards Family 19 9* (5) 7 (5) this would support the island rule. Birds Genus 223 90** (71) 73 (71) At the family level we adjusted the protocol to control for Birds Family 86 24 (21) 21 (21) clade species richness, so that rather than each species Birds Order 19 3 (3) 6 (4) contributing equally to the family mean, each species contrib- Mammals Genus 91 29 (36) 38 (35) uted equally to the genus mean and each genus then Mammals Family 39 9 (11) 10 (12) contributed equally to the family mean. The same procedure Mammals Order 12 4 (3) 2 (3) was repeated at the order level with the addition of taking the Mammalsà Genus 101 35 (40) 41 (39) mean across families in an order. Tests with species treated Mammalsà Family 47 14 (14) 12 (14) Mammalsà Order 14 5 (3) 3 (3) independently (i.e. simple means of all species in a family or Mammals [BM] Genus 91 28* (35) 38 (35) order) gave qualitatively the same results (not shown). Mammals [BM] Family 39 9 (11) 10 (11) Using the modified mammal tree we located nodes that Mammals [BM] Order 12 4 (3) 2 (3) represented a partition between a solely insular and a solely Mammalsà [BM] Genus 99 33 (37) 41 (37) mainland clade and estimated the mean body size for each Mammalsà [BM] Family 46 15 (14) 12 (14) clade. Clades including polytomies were excluded. The sister Mammalsà [BM] Order 14 6 (3) 3 (3) clades we identified are shown as Appendix S2. As the clades involved in each island versus mainland comparison vary in *, **Denote statistical significance at the a = 0.1 and 0.01 levels, respectively. age, then under a Brownian motion model of evolution the The median expected values derived from our randomizations are in expected variance of the mean values of these clades is expected parentheses. to vary, violating an assumption of SMA regression (Welch, àIncluding extinct species. [BM] denotes analyses conducted using 2009). Consequently, we estimated the statistical significance Brownian motion simulations rather than randomizations. of a departure from a 1:1 relationship between the size of Note that because we only have phylogenetic data for c. 92% of island and mainland taxa by applying 10,000 randomizations mammalian species observed numbers of size extremes can differ of the identity of insular and mainland clades using the between non-phylogenetic and phylogenetic analyses.

Journal of Biogeography 38, 89–100 93 ª 2010 Blackwell Publishing Ltd S. Meiri et al.

(a) (b) scale) 10

Figure 2 Standardized major axis regression

of mean body size [log10-transformed snout–vent length (SVL) in mm] on islands

Insular mean SVL (log versus continents for species in lizard genera (a) and families (b). The dashed line has a slope of 1 and an intercept of 0. The solid line represents the standardized major axis Continental mean SVL (log scale) 10 regression slope estimate.

(a) (b) (c) scale) 10 Insular mean mass (log

Continental mean mass (log10 scale)

Figure 3 Standardized major axis regression of mean body size (log10-transformed mass, in g) on islands versus continents for species in bird genera (a), families (b) and orders (c). The dashed line has a slope of 1 and an intercept of 0. The solid line represents the standardized major axis regression slope estimate.

Birds respectively (Fig. 3a,b). The slope at the order level, however, was significantly shallower than 1 (SMA slope = 0.76, 95% Of 8069 bird species in our dataset, 1347 are insular endemics CI = 0.66–0.88, r = )0.70, P < 0.01; P < 0.01; (we have maximum mass data for all, and for 7552, including randomization Fig. 3c), even when ratites are excluded (SMA slope = 0.78, 1268 insular endemic species, we have data on mean size; 95% CI = 0.64–0.95, r = )0.56, P < 0.05; P < Appendix S1b). In 90 out of 223 avian genera the largest randomization 0.05). member of the clade is an insular endemic. This is significantly more than expected under our randomizations (median expected = 71; P < 0.01, Table 1). However, at the family Mammals and order levels (see size frequency histograms in Appen- dix S3b) the largest member of a clade is no more often an Of 3961 extant mammal species, 670 are insular endemics (778 insular endemic than expected at random. The frequency with of 4213 when extinct species are included). The frequency of which the smallest member of a clade is an insular endemic insular endemics that are either the largest or smallest does not depart from the null expectation for any taxonomic members of their clades does not depart from the null level. Moreover, when we repeated the analysis at the genus expectation derived by randomization at any taxonomic level, level using the maximum rather than mean body size (data are either including or excluding extinct taxa (Table 1, Appen- the maximum reported for a species in Dunning, 2008), dix S3c). neither the frequency of gigantism nor dwarfism departed In agreement with the results from randomizations, the from the null expectation (67 observed insular maxima across frequency of gigantism and dwarfism tended not to exceed the 219 genera, median expected = 71, P = 0.53). null expectation generated under a single-rate Brownian model There was no evidence for the island rule at the genus and on the mammalian phylogeny. This was true for all taxonomic family level in birds, with slopes equal to 1.00 and 0.98, levels, both including and excluding extinct species, except for

94 Journal of Biogeography 38, 89–100 ª 2010 Blackwell Publishing Ltd Island vertebrates and body size extremes extant mammals at the genus level, where the frequency of but not using randomizations (P = 0.155; Fig. 5a). Restricting gigantism was marginally lower than expected (P = 0.1). the analysis to insular versus mainland sister species, we get a Mammals show a general tendency to follow the island rule slope consistent with the island rule using both tests (n = 57, at the genus level. The observed slope of mean insular clade slope = 0.870, 95% CI = 0.81–0.93, r = )0.49, P < 0.01; mass versus mean continental clade mass is significantly less Prandomization < 0.05, Fig. 5b). than 1 for genera both including and excluding extinct species (extant only: SMA slope = 0.96, 95% CI = 0.93–0.99, r = DISCUSSION )0.24, P < 0.05; Prandomization < 0.05, Fig. 4a; extant + extinct: slope = 0.92, 95% CI = 0.89–0.96, r = )0.41, P < 0.01; The largest species in bird and lizard taxa tend to be insular

Prandomization < 0.05, Fig. 4d; see also Fig. 1c). The slope for more frequently than expected were insular status assigned to families is not significantly different from 1 (slope = 1.01, 95% species at random. Interestingly, however, this holds within CI = 0.95–1.08, and 0.95, 95% CI = 0.89–1.01, with and bird genera (but not when species maximum rather than mean without extinct species, respectively, Fig. 4b,e). The slope for masses are used), whereas lizards only show gigantism among orders likewise is not significantly different from 1 families. Furthermore, the lizard giants are often the result of (slope = 1.01, 95% CI = 0.74–1.37, and 0.87, 95% CI = insular radiations (e.g. Hoplodactylus, Gallotia, Cyclura)on 0.76–1.05, with and without extinct species, respectively; islands lacking mammalian carnivores (here New Zealand, the Fig. 4c,f). Canaries and the Antilles, respectively). Such absence of When analyses were conducted using the mammalian mammalian predation has been hypothesized to promote phylogeny, regressing mean body sizes within insular clades lizard gigantism by allowing for more foraging, as less time is on the mean size within their mainland sister clades returned a spent hiding from predators, and by enabling lizards to evolve slope significantly shallower than 1 using SMA (n = 91, the role of top predators (Case, 1982; Meiri, 2008). In birds, slope = 0.931, 95% CI = 0.877–0.987, r = )0.25, P < 0.01), the largest members of genera that are insular seem to be quite

(a) (b) (c) scale) 10

(d) (e) (f) Insular mean mass (log

Continental mean mass (log10 scale)

Figure 4 Standardized major axis regression of mean body size (log10-transformed mass, in g) on islands versus continents for species in mammalian genera (a, d), families (b, e) and orders (c, f). Plots (a)–(c) are for extant taxa only and (d)–(f) include extinct taxa (see Materials and Methods). The dashed line has a slope of 1 and an intercept of 0. The solid line represents the standardized major axis regression slope estimate.

Journal of Biogeography 38, 89–100 95 ª 2010 Blackwell Publishing Ltd S. Meiri et al.

(a) (b) scale) 10

Figure 5 Standardized major axis regression

of mean body size (log10-transformed mass, in g) on islands versus continents within (a) mammalian sister clades and (b) a subset of the data in (a): only sister species [only clades

Insular mean mass (log in (a) where both mainland and insular sample sizes are 1]. The dashed line has a slope of 1 and an intercept of 0. The solid line represents the standardized major axis Continental mean mass (log scale) 10 regression slope estimate. evenly distributed between continental shelf, volcanic and 2000). Thus, the apparent tendency for smaller mean size in continental plate islands (e.g. the Philippines, New Guinea, insular members of large-bodied avian orders may be a result Tasmania, Hawaii and New Zealand). This suggests that release of human-mediated extinction (Steadman, 2006; Pavia, 2008) from predation on islands has often promoted gigantism in rather than a feature of natural insular evolution. lizards and perhaps gigantism associated with flightlessness in The finding that bird genera harbour more insular giants birds (e.g. the New Zealand moas, Sylviornis; Russell, 1877; than expected by chance is surprising, given that the mean size McNab, 1994), but perhaps a different mechanism drove of species within bird genera does not seem to differ between gigantism among birds that retained their power of flight (e.g. islands and mainlands (Fig. 2a). A thorough study of the avian high population density; Blondel, 2000). subfossil record may even reveal that when extinct taxa are Size extremes in insular mammals show no departure from included a similar pattern will be revealed within families and null expectations. However, mammals conform to the island orders. rule at the genus level, especially when fossil species are A common explanation for insular gigantism in birds and included. This pattern also emerges when we compare sister reptiles (e.g. elephant birds, moas, Komodo dragons and the species, a better test of size evolution than comparing clade giant skinks of Cape Verde and New Caledonia) is that they members ignoring their phylogenetic affinities. have evolved large size on islands with no mammalian In all three taxa, deviations from a slope of 1 seem to stem competitors or predators (Russell, 1877; Case, 1978; McNab, from small (mammals and birds) or large (lizards) members of 2002; Meiri, 2008). While we view this as a highly likely generally large-bodied forms (e.g. small elephants, artiodactyls, explanation, we are not sure it can explain our finding that ratites and ducks, large iguanas). Extinct mammals show the island birds tend to be the largest members of their genera most drastic cases of dwarfism. However, many of the recently more often than is expected by chance. Our impression from extinct insular lizards and birds are extremely large (Pregill, the data is that these largest members of avian genera are 1986; Blondel, 2000) and extinction in these taxa was probably mostly found on large islands, rich in bird, reptile and often much more prevalent on islands than on mainlands, whereas mammal species. Being classified as congenerics of mainland extinctions of large mammals were common in mainland forms, insular giants seldom occupy niches vacated by settings (Barnosky et al., 2004). Thus in early Holocene times mainland mammals, and usually differ relatively little from there were giant insular birds in orders now exhibiting an the size of their mainland relatives. Currently we are unable to overall tendency for small sizes on islands. Indeed very large, sufficiently explain why this pattern prevails, or why it holds recently extinct, insular birds include members of the Falcon- only for birds, and only within genera, and note that species iformes (e.g. Amplibuteo, Harpagornis moorei, Circus eylesi; maximum sizes [probably an inferior size measure because it is Worthy et al., 2002; Sua´rez & Olson, 2007) and Strigiformes more sensitive to sample size (Meiri, 2007) but representing (e.g. Tyto riveroi, Ornimegalonyx oteroi; Alcover & McMinn, about 7% more species (Dunning, 2008)] do not show the 1994), ratites (Dinornis, Aepyornis; Worthy et al., 2002), same trend. Anseriformes (e.g. Cygnus falconeri and the ‘very large Hawaii The evidence we find for the island rule in mammals goose’; Milberg & Tyrberg, 1993; Paxinos et al., 1999), emerges primarily via insular dwarfism in large taxa. Curi- Ciconiiformes (Threskiornis solitarius, perhaps a Pelecaniform; ously, the tendency of large mammals to dwarf on islands (see Mourer-Chauvire et al., 1995), Gruiformes (Diaphorapteryx also Raia et al., 2010), which is corroborated by our phylo- hawkinsii, perhaps Aptornis; Holdaway, 1989; Raia, 2009), genetic tests, and when fossils are included, is also linked to the Galliformes (e.g. Megavitiornis, perhaps Sylviornis; Steadman, absence of predators and competitors, and seems more 2006) and Columbiformes (Raphus cucullatus, Pezophaps prevalent in herbivores than in carnivores (Raia & Meiri, solitaria, Natunaornis gigoura; Steadman, 2006; Worthy, 2006). McNab (2002) has claimed that gigantism in insular

96 Journal of Biogeography 38, 89–100 ª 2010 Blackwell Publishing Ltd Island vertebrates and body size extremes birds is more likely in herbivorous taxa. Additionally, in lizards agents such as resource abundance, predation and competi- insularity is often associated with large size and herbivory tion, which in turn differ across different islands. (Troyer, 1983; Meiri, 2008). Gigantism may be favoured where resources are abundant (McClain et al., 2006), and the size of ACKNOWLEDGEMENTS large carnivorous vertebrates may depend on the size of available prey; thus islands lacking large herbivorous mammals We thank Liz Butcher and Barbara Sanger from the Michael are likely also to lack large carnivores. Because mammals can Way Library for their enormous help in obtaining literature grow much larger than either birds or lizards, one might say sources for data used in this work. Felisa Smith kindly that even the largest avian and reptilian predators, Haast’s provided us with the latest version of the ‘Integrating eagle and the Komodo dragon, are not large predators Macroecological Pattern and Processes across Scales’ (IMMPS) compared with large mammalian carnivores. Thus low preda- working group mammalian mass database. We thank Ian tion and competition pressures on islands may tend to Owens for valuable discussion and Mark Lomolino, Craig produce both relatively small mammals and relatively large McClain, John Welch and two anonymous referees for very lizards. helpful comments on earlier versions of this manuscript. The nature of the islands that we study, in terms of their area and isolation, climate, geology (e.g. whether they are part REFERENCES of the continental shelf, part of a tectonic plate or volcanic) and biogeographic settings (e.g. realm, ocean) may all affect Adler, G.H. & Levins, R. 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Journal of Biogeography 38, 89–100 99 ª 2010 Blackwell Publishing Ltd S. Meiri et al.

BIOSKETCHES

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 and vertebrate evolution.

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 the effect of ecological interactions.

Albert Phillimore is an Imperial College Junior Research Fellow and is interested in the influences of ecology on evolution and speciation.

Author contributions: A.B.P., P.R. and S.M. conceived the ideas and collected the data; A.B.P. analysed the data; S.M. led the writing.

Editor: K.C. Burns

100 Journal of Biogeography 38, 89–100 ª 2010 Blackwell Publishing Ltd