The smallest primates

News and Views The smallest primates Daniel L. Gebo Department of Anthropology, Northern Illinois University, DeKalb, IL 60115, U.S.A. E-mail: dgebo@niu.edu Marian Dagosto Department of Cell and Molecular Biology, Northwestern University Medical School, Chicago, IL 60611, U.S.A. E-mail: m-dagosto@nwu.edu K. Christopher Beard Section of Vertebrate Paleontology, Carnegie Museum of Natural History, Pittsburgh, PA 15213, U.S.A. E-mail: Eosimias@alphaclp.clpgh.org Tao Qi Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, P.O. Box 643, Beijing, 100044, People’s Republic of China Journal of Human Evolution (2000) 38, 585–594 doi:10.1006/jhev.2000.0395 Available online at http://www.idealibrary.com on Among living members of the Order Primates, taxa weighing less than 50 g are extremely rare (Jungers, 1985; Atsalis et al., 1996). Moreover, all living species of primates in this small size range are members of the Malagasy radiation of strepsirhines (Genus: Microcebus; Atsalis et al., 1996). This was not the case, however, for the diverse primate fauna from the middle Eocene Shanghuang fissure-fillings of southern Jiangsu Province, China (Beard et al., 1994). Primate postcranial elements from the Shanghuang fissure-fillings show that a diversity of tiny haplorhine primates (about six species) inhabited eastern China during the middle Eocene. Among these diminutive Chinese taxa are two species that considerably extend the known size range of primates. The distribution of body mass for the entire Shanghuang primate fauna is distinct from that of other known primate faunas, both living and extinct. The earliest phases of haplorhine phylogeny, including the initial diversification of tarsiiform and anthropoid primates, probably occurred at or below the 0047–2484/00/040585+10$35.00/0 lower limits of body mass found in living primates. The smallest living mammals are species of the Insectivora, Chiroptera, Rodentia, and Dasyuridae (Nowak & Paradiso, 1983; Churchfield, 1996). Sorex minutissimus (1·5– 3 g), Suncus etruscus (1·5–2 g), Rynchonycteris naso (2·1–4·3 g), Salpingotulus (3 g), Micromys (5–9 g), and Mus (2·5–12 g) are among the tiniest living mammals (Nowak & Paradiso, 1983; Churchfield, 1996). Within an estimated body mass of only 1·3 g, the early Eocene insectivore Batodonoides vanhouteni may actually have exceeded the lower limits of body mass found in living mammals (Bloch et al., 1998). No living primates approach this small size. Microcebus myoxinus, the smallest living primate, weighs 26–37 g, and other species of this genus range from 32–77 g (Atsalis et al., 1996). At 125 g Cebuella is the tiniest living anthropoid. Tarsiers are the smallest extant haplorhines, ranging from 90–150 g. The body mass of the smallest species, Tarsius pumilus is unknown, although it is unlikely to be less than 50 g.  2000 Academic Press 586 . .  ET AL. Figure 1. Shanghuang calcanei IVPP V 11848 (center) and IVPP V 11847 (right) compared to Microcebus murinus (Left, NIU specimen), one of the smallest living species of primates (60 g). Scale in millimeters. See Table 1 for measurements. Known fossil primates do not significantly exceed the range in body mass shown by living primates. Altanius orlovi, estimated at 21–23 g based on molar size (Conroy, 1987), is possibly the smallest fossil primate, but opinions are varied as to whether this species is a primate or a plesiadapiform (Rose et al., 1994). The omomyids Pseudoloris, Teilhardina, Tetonius, Uintanius, Trogolemur, Uintalacus, Utahia, Washakius and Anemorhysis are the smallest undoubted fossil primates described to date. If all primate, prosimian only, or strepsirhine only regression models are used to estimate body mass from molar size, these species are approximately the size of living Microcebus, but not smaller (Gingerich, 1981; Conroy, 1987; Dagosto & Terranova, 1992). However, if a tarsier only regression model is used, some of these species may have been as small as 15 g (Gingerich, 1981). The smallest fossil anthropoids are Eosimias [67–179 g (Beard et al., 1994, 1996)], Algeripithecus [150– 300 g (Godinot & Mahboubi, 1992)] and Qatrania wingi [160–278 g (Conroy, 1987)]. Primate postcranial elements from the middle Eocene Shanghuang fissure-fillings of southeastern China (Beard et al., 1994) place new limits on the range of body mass in this order, and suggest that major primate clades may have originated below the limits of body mass in living primates. IVPP V 11847 and IVPP V 11848 (IVPP=Institute of Vertebrate Paleontology and Paleoanthropology) are calcanei from Shanghuang Fissures A and D, respectively (Figure 1). The vertebrate faunas from these fissures have been estimated to date to approximately 45 ma on purely biostratigraphic evidence (Wang & Dawson, 1992; Beard et al., 1994). Both calcanei are complete, and exhibit all of the features typical of primates (Gebo, 1988), allowing them to be securely assigned to this order. The epiphysis of the heel is fused to the rest of the bone in both specimens, indicating that these bones are from adults. These specimens pertain to new, and as yet unnamed, species. The Shanghuang calcanei are attributed to Haplorhini on the basis of the morphology of the posterior calcaneal facet, which is relatively short and broad, unlike in adapiforms where it is long and narrow. Both of these calcanei are also far outside the size range represented by Shanghuang adapids. IVPP V 11847 is morphologically similar to calcanei of North American    omomyids. However, IVPP V 11847 probably pertains to a different haplorhine taxon because the only omomyid currently known from Shanghuang is Macrotarsius [900– 1221 g (MacPhee et al., 1995)], a taxon likely to have been larger than that represented by IVPP V 11847 by roughly two orders of magnitude. IVPP V 11848 differs morphologically from IVPP V 11847 in having a much broader distal segment, and a calcaneocuboid joint in which the pivot is shifted medially. These morphological differences exceed those found in living and fossil primate families, suggesting that IVPP V 11848 and IVPP V 11847 represent distinctly different haplorhine clades. The anatomical distinctions of the IVPP V 11848 specimen are shared with anthropoids, suggesting attribution to Anthropoidea, probably the Eosimiidae. Dental remains have not yet been allocated to either of these small taxa. Compared with other primates, the most remarkable aspect of these bones is their small size. IVPP V 11847 is only 4·0 mm in length, while IVPP V 11848 measures 4·25 mm (Table 1, Figure 1). Both Shanghuang calcanei are considerably smaller than those of any extant or fossil primate for which the relevant anatomy is known (Table 1). The entire length of the IVPP V 11847 and IVPP V 11848 calcanei is only as long as the combined heel and posterior facet lengths of calcanei belonging to Microcebus murinus, a 60 g primate (Figure 1). Comparisons of total calcaneal length are complicated by the variable degree to which the distal part of the calcaneus is elongated in primates. Microcebus, for example, has a particularly long distal calcaneus (about 65% of total length). The Shanghuang specimens exhibit more moderate distal elongation (52–53%), comparable to that of omomyids. However, all other dimensions of the calcaneus are also considerably smaller than in other known primates (Table 1). 587 Several measurements of the calcaneus prove to be reasonable estimators of body mass in prosimian primates (Dagosto & Terranova, 1992). Using these equations, the body mass of IVPP V 11847 is predicted to be 9·5–16·4 g (Table 2). Similar estimates for IVPP V 11848 range from 13·3– 23·6 g. The Chinese fossils are beyond the size range of the extant primates used to construct the model. Therefore, classical calibration may be more appropriate in this instance (Hens et al., 1998). Estimates from this technique are slightly lower than those derived from inverse calibration (Table 2). The factor score from a first principal component analysis of all calcaneal variables was also used to predict body mass (Payseur et al., 1999). This method yields estimates of 10·6 g for IVPP V 11847 and 17·2 g for IVPP V 11848 (or 8·1 g and 12·5 g, respectively, using classical calibration). Similarly, head and body length can be predicted from calcaneal size. For IVPP V 11847, the first principal component yields an estimate for head and body length of 60–70 mm. The same estimate for IVPP V 11848 is 70–80 mm. These values are less than half those for the smallest living primate, Microcebus myoxinus (Atsalis et al., 1996), but are similar to those of shrews and mice weighing about 15 g (Churchfield, 1996). All of the preceding models are based on extant strepsirhines. Because neither of these fossils belongs to this clade, they may not follow the same scaling trends. In other fossil primates, especially omomyids, body mass estimates based on postcrania do not always agree with estimates based on teeth (Dagosto & Terranova, 1992). Table 2 provides body mass estimates for other small primates based on calcaneal variables. It is clear from both the body size estimates and from the absolute measurements (Table 1) that, by any standard, the Shanghuang primates are the smallest known. Mammals of very small size face a variety of physiological constraints (Calder, 1984; 588 Table 1 Measurements of the calcaneus (in mm) for the Shanghuang fossils, extant Microcebus, and some small omomyids* Microcebus ?rufus Microcebus murinus Teilhardina belgica Arapahovius gazini Absarokius abbotti Shoshonius cooperi Tetonius sp. Washakius insignis 8·58 2·33 5·27 1·77 1·58 1·67 1·57 2·48 7·10 2·46 3·63 1·64 1·86 4·81 9·80 2·87 5·58 1·95 2·28 3·38 9·79 3·25 5·20 2·23 2·22 2·32 1·55 4·95 4·25 1·80 2·20 1·20 0·85 1·25 0·90 2·22 10·09 2·55 6·20 1·87 1·97 1·73 1·69 4·95 4·00 1·55 2·10 1·15 0·75 1·00 0·80 3·56 10·00 3·35 2·56 1·80 1·54 3·34 2·61 2·18 2·45 2·51 2·12 1·90 *For the extant species and omomyids, the mean is given. Designations C1–C7 refer to the illustration of measurements in Dagosto & Terranova (1992), Figure 1. The mean body mass of Microcebus rufus is 42 g and 59 g for Microcebus murinus (Atsalis et al., 1996). A single calcaneus of Microcebus ?myoxinus from Kirindy (uncatalogued specimen from the Field Museum, Chicago) measures 8·93 mm in length. The mean body mass of this species is 30 g (Atsalis et al., 1996). ET AL. IVPP V 11848 . .  Area of lower first molar Calcaneal length (C1) Calcaneal width (C2) Distal length Posterior calcaneal facet length (C3) Posterior length (C7) Calcaneocuboid width (C6) Calcaneocuboid height (C5) IVPP V 11847 Table 2 Body size estimates (g) from the strepsirhine regression equations in (Dagosto & Terranova, 1992)* Measurement Area of lower first molar Calcaneal width (C2) PCA (C2–C6, index 6) Average of calcaneal estimates from inverse calibration Average of calcaneal estimates from classical calibration IVPP V 11848 15·4 (12·0–19·8) 10·9 16·4 (12·2–22·0) 11·1 9·5 (5·9–14·9) 4·9 9·7 (7·2–13·0) 9·3 13·1 (7·2–26·9) 7·0 10·6 (6·6–17·1) 8·1 12·5 23·6 (18·3–30·4) 17·2 18·5 (13·8–24·7) 13·8 13·3 (8·5–21·1) 7·2 22·2 (17·8–27·8) 17·6 15·9 (11·9–21·4) 11·8 17·2 (10·6–24·8) 12·6 18·5 8·6 13·4 Microcebus murinus Teilhardina belgica Absarokius abbotti 65·9 (50–86) 78·0 (62–99) 222·0 (170–291) 60·4 (47–78) 54·5 (42–70) 84·7 (66–109) 131·9 (102–170) 131·9 (102–170) 58·2 (43–78) 40·6 (30–54) 65·3 (49–88) 122 145 58·6 (37–93) 108·5 (69–171) 77·0 (49–122) Washakius insignis 138 (113–169) (91–164) 51·3 (41–64) 88·9 (71–111) 59·8 (45–80) 94·2 (70–127) 61·3 47·6 69·5 109·1 Tetonius homunculus 232 (194–277) (108–194) 95·8 (77–120) 124·2    Length of posterior calcaneal facet (C3) Calcaneocuboid Ht (C5) Calcaneocuboid facet width (C6) Index 6 (=C5C6) IVPP V 11847 *The prediction and the 95% confidence interval is given. For each calcaneal variable, the top line gives the estimate from inverse calibration, the second line gives the estimate from classical calibration. All raw values are multiplied by the appropriate correction factor following (Sprugel, 1983). All correction factors are less than 5%. 589 590 . .  Alexander, 1996; Miller, 1996) and these allow us to draw further paleobiological inferences for the tiny haplorhine primates from Shanghuang. A very high metabolic rate (Kleiber, 1961; Alexander, 1996), and therefore a diet rich in high caloric items such as insects, nectar or fruit is likely (Kay, 1984; Kay & Covert, 1984; Atsalis, 1999). The gut would probably be minimally specialized (Chivers & Hladik, 1984) with a high surface area, allowing water and other nutrients to be absorbed rapidly (Martin, 1990). Heat and water exchange would be a significant problem for such tiny primates (Porter & Gates, 1969; Alexander, 1996). Life history factors are also influenced by size. Small mammals have fewer but relatively larger neonates and a relatively longer gestation time than their larger relatives (Purvis & Harvey, 1996). Given the longer gestations and fewer offspring reported for living haplorhines (Martin, 1990), this implies a small ancestral condition like that found at Shanghuang. With small size also comes an increased risk of predation, especially by raptorial birds (Goodman et al., 1993). The intermembral index (IMI) of these species is probably low, because IMI generally decreases with size among primates (Jungers, 1985). A low IMI implies frequent leaping by both IVPP V 11847 and IVPP V 11848. Based on available postcranial and dental remains, we estimate that the Shanghuang fauna contains 15–19 species of primates. We inferred the body masses of these species using the same techniques described above. Figure 2 and Table 3 compare the size distribution of the Shanghuang primate fauna with those of other communities of living and extinct primates. The Shanghuang fauna is apparently unique in including so many very small (<100 g) species of primates, while lacking species of large size (>1000 g). This distinction holds with respect to both living and fossil primate faunas, including one of similar age (Bridger ET AL. Basin, Wyoming). Being smaller allows correspondingly small home ranges, permitting many taxa to pack into these ancient forests. With so many small, closely related and sympatric primates occurring in the ancient forests at Shanghuang, competition may have been a significant problem. Intense competition normally promotes a diversity of biological niches including a variety of dietary preferences, diurnal and nocturnal activity patterns, and levels of forest use in primates (Charles-Dominique, 1977). One explanation for the unique distribution of body mass shown by the Shanghuang primate fauna is that this assemblage samples a portion of the primate evolutionary tree that is missing from other well-sampled fossil primate faunas (and completely unrepresented among extant primate diversity). Primate taxa already described from Shanghuang include basal tarsiids and anthropoids, in addition to the adapiforms and omomyids that characterize many other Eocene primate faunas (Beard et al., 1994). It is impossible to establish the precise phylogenetic positions of the tiny haplorhine taxa represented by IVPP V 11847 and IVPP V 11848 on the basis of the limited anatomical evidence. Nevertheless, these specimens demonstrate that haplorhine primates smaller than any living primate inhabited southeastern China during the middle Eocene. Furthermore, these tiny haplorhines encompassed at least a moderate degree of taxonomic diversity. Because basal tarsiids and basal anthropoids are both represented at Shanghuang, at least part of the radiation of tiny haplorhines known from this site may pertain to either or both of these clades. Indeed, based on regressions of body mass against molar area (Gingerich, 1981), the early tarsiid Tarsius eocaenus from Shanghuang (Beard et al., 1994) weighed only 29 g, which is also less than any living primate. Undoubted anthropoids of such diminutive size have not yet been reported from Shanghuang, although Eosimias was Shanghuang, China Bighorn Basin, Wyoming 12 10 10 10 8 8 8 6 6 6 4 4 4 2 2 2 0 2 3 4 5 6 7 8 9 10 Ranomafana, Madagascar 12 0 2 3 4 5 6 7 8 9 10 Manu, Peru 12 0 10 10 8 8 8 6 6 6 4 4 4 2 2 2 2 3 4 5 6 7 8 9 10 0 2 3 4 5 6 7 2 3 8 9 10 0 4 5 6 7 8 9 10 9 10 Makoukou, Gabon 12 10 0 Bridger Basin, Wyoming 12 2 3 4 5 6 7 8    Number of species 12 ln body mass (grams) Figure 2. Body size distribution (x axis is natural log of body mass) of Shanghuang primates compared to two other Eocene fossil localities (Bighorn and Bridger Basins, Wyoming) and three extant primate communities from South America (Manu), West Africa (Makoukou), and Madagascar (Ranomafana). A figure of Microcebus indicates the bin for the smallest living primate (30–60 g). Body mass data for the living primates are from Fleagle (1999), Waser (1987), and Wright (1992). Species lists for the Bighorn Basin from (Bown & Rose, 1987, 1991; Gebo et al., 1991) and the Bridger Basin from (Gunnell, 1997). Size estimates for the Wyoming fossil primates are derived from dental dimensions using the prosimian regression equation of Conroy (1987). This may overestimate size compared to the postcranial dimensions used for the Shanghuang primates, however, no dentally known primate from the Wyoming fossil localities is smaller than Microcebus in the area of the first lower molar. 591 592 . .  ET AL. Table 3 Body mass distribution for some extant and fossil primate communities* Manu Taxon Makoukou Body mass Taxon Body mass Taxon Extant communities Cebuella pygmaea Saguinus fuscicollis Callimico goeldii Saguinus imperator Callicebus moloch Aotus trivirgatus Saimiri sciureus Pithecia monachus Cebus albifrons Cebus apella Lagothrix lagotricha 110 343 468 474 800 800 900 2110 2800 3000 7020 Galagoides demidovii Galago alleni Euoticus elegantulus Arctocebus calabarensis Perodicticus potto Cercopithecus talapoin Cercopithecus cephus Cercopithecus pogonias Cercopithecus neglectus Cercopithecus nictitans Cercocebus galeritus Ateles paniscus Alouatta seniculus 8000 8000 Cercocebus albigena Colobus guereza Papio sphinx Shanghuang Taxon Fossil communities NH1 E1 T1 E2 P1 NH2 P2 E3 P3 NH3 T2 E4 P4 E5 P5 Adapoides troglodytes NH4 Adapiform Macrotarsius macrorhysis Ranomafana 60 269 300 306 836 1100 2900 3000 4000 4200 5260 6020 9200 11,500 Microcebus rufus Cheirogaleus major Eulemur fulvus Eulemur rubriventer Varecia variegata Hapalemur griseus Hapalemur simus Hapalemur aureus Lepilemur microdon Avahi laniger Propithecus diadema Daubentonia madagascariensis Big Horn Basin Body mass Taxon 12 17 26 28 28 35 53 63 71 79 81 89 107 110 123 200 353 421 800 Teilhardina tenuiculus Teilhardina demissa Arapahovius advena Teilhardina crassidens Tatmanius szalayi Anaptomorphus wortmani Teilhardina americana Anemorhysis pattersoni Teilhardina sp. Chlorohysis Tetonius sp. Steinius vespertinus Strigorhysis bridgerensis Pseudotetonius ambiguus Tetonius matthewi Absarokius metoecus Absarokius abotti Cantius ralstoni Cantius trigonodus Cantius feretutus Cantius frugivorous Cantius abditus Pelvcodus jarrovi Body mass 49 362 2180 1940 3520 670 1300 1390 800 1030 5830 2490 Bridger Basin Body mass Taxon 68 78 80 86 87 89 92 98 100 120 139 151 155 161 180 190 204 1300 2000 2000 2800 3000 4500 Trogolemur myodes Uintanius ameghini Sphacorhysis burntforkensis Trogolemur amplior Uintanius rutherfurdi Anaptomorphus aemulus Washakius insignis Hemiacodon gracilis Omomys carteri Wyomomys bridgeri Anaptomorphus westi Ageitodendron matthewi Gazinius bowni Gazinius amplus Smilodectes gracilis Notharctus tenebrosus Notharctus pugnax Notharctus robustior Body mass 65 70 78 85 94 133 155 300 310 320 415 493 600 875 2100 2500 3000 6900 These data are used to construct Figure 3. For the extant communities, species lists are from Waser (1987) and Wright (1992). Species body mass is from these sources and Fleagle (1999). In cases where there is significant sexual dimorphism, the female body weights are given. For the fossil communities, body mass estimated from tarsal bones is given in bold, otherwise, the estimate was made from first lower molar area following Conroy (1987). If these data were unavailable, the estimates in Fleagle (1999) were used. The number of taxa for Shanghuang is documented in Gebo et al. (in prep) (E=eosimiid; NH=new haplorhine; P=protoanthropoid; T=tarsiid).    certainly small (body size estimate: 67–158 g). 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