10 Paleoecology of the Paucituberculata and Microbiotheria (Mammalia, Marsupialia) from the late Early Miocene of Patagonia
Mar/a Alejandro Alu!ilo, Edgardo Ortiz-JaureguizaT, anti Adriana M. Candela
Abstract ami li sis de los result ados de las mas as corporales y [a This chapter presents a paleoecological an alysis of non dietas, se reconocieran diversos nichos ecologicos: camivorous Sanlacrucian marsupials of the orders Paucituber pequen os a medianos insectivoros. pequenos a medianos culara and Microbiothelia. Different ecological niches are insecliv oros~ fru g i v oros y medianos a grandes ft1Jgiv oros. infen-ed [Tom estimates of bcx:Iy mass, diet, and iocomOior Nuestros resultados nos pemliten coneluir qu e lo s Pauej behavior. Body masses were estimated using a regression tu berculata y los Microbiothe ria de la FOlmaci6n Santa analysis based on living marsupials. Possible dietary prefer Cruz constituyen ull agregado ecologicamente diverso ences were explored by an analys is of the developmeut ofmolar que habit6 zonas boscosas. desarrolladas bajo un clima shearing crests. Inferences about locomotor behaviors of some calid o y con lIu vias estac ionales. ESlas zonas habrian spec ies with we ll -preserved postcran iaJ skeletal remains were ofrecido una amplia diversidad de recursos fanlo espa deJived from a publ is hed morphofunctional analysis. From the ciale!-. como troficos para los diversos ni chos ecologicos wide range of estimat.ed body masses and diet several niches de los marslipiaies no carn lvoros. Nuestfa reconstrucci6n were infened: small- to medium-sized insecti vores, small- to paleoambiental es compatible con la ex isrencia de hetero medium-sized insectivore-frugivores, and medium- to large geneidad arnbie nl al dmante el Sanl 156 Paleoec% RY of Santacrucian Pauciruherculata alld Microhiotheria 157 ,------______Monol rem ~l~ 1l1e fossiJ record of Paucitubercul a[a and M icrobiotheria ,--_------Vmcelesfes indicates that these marsupials had a wid er geographic Euthaflll disllibution and hi gher taxonomic di versity than those of ,------DeJlellleriClum the present (Abell o, 2007; G01n ef al., in press) . The oldest· ,-______Pucadff/phys known Paucituberculata and Microbiotheria date from the ,------CMolph lll1 orpllta Paleocene and include fonns such as the paucituberculatan ,-______Paucltubercullta Bardalestes Goin , Candela, Abello and Oli veira, 2009 ,-____ Oas ywomorphla (ltaboraian Age, Argentina; Goin el al. , in pres s) and the ,-___ Pernmella microbiotherian Mirand.arheriw71 (Paula Couto, 1952) from Microbiother/a Brazil (Itaboraian Age; Goi n e( al. , in press). Bolh groups Diprolodon tJa achieved their hi ghest taxo nomi c di versity in the Early Mi ocene Colhuehuapian ~nd Santacrucian Ages, but the Fig. 10.1. Phylogenetic Iree showing the relationships of li ving marsupial oruers (modified from HoroviTz and Srinchez~ Villagra. 2003 ). in fe n'ed cladogenetic events that gave rise to the Miocene fOims seem to hav e OCC UlTed during the Oligocene (Abello, phylogenetic studies based on molecular or combined data 2007; Goin el al. , 2010). By the Early Miocene, micro (e.g. , Nilson et al., 2004; Asher et aI., 2004; Beck, 2008; biotherians are represented by nine species belonging to Meredith ef 0/., 2008), as well as some morphological Microbiotheriidae. At [he same time, paucitu berculatans studies based on cranial , postcranial, and soft tissue are represented for 23 species gro uped among Caenol estj anatomy (Horovitz and Sanchez· Villagra, 2003), indici:lte dae, Pi chipilidae, Palaeothenti dae, and Abderitidae. that Paucituberculata is the sister group of Au stralidelphia. Despite the abundant representation of small marsup ia ls Microbi otherialls and pallcituberculatans are poorly (parti cularly paucituberculatans) in the Early Miocene represented in presenl.day ecosyste ms (Flores, 2006a, b; (Bown "nd Fl eagle, 1993; Abello, 2007), they are mainly PatterSo n, 2007; Patterso n and Rogers, 2007). The only known by mandibular and max illalY remains and isolated extant microbiotherian is the so-called "monito del mome" leeth. Consequently, the reconstructions of cerrain paleo (Dromiciops gliroides), a small insectivorous marsupi al ecological aspects (e.g_ body size, diet) have been de rived endemic to the temperate forests of so uthern Chi Ie and from the sLud y of dental remains. Argentina, associated wi th (he southern beech forests Several ecological niches have been identified among (Nothofagus) and South American mountain bamboos Paucituberculala (Dumont el 01., 2(00): small insectiv ores (Chusquea) (Hershkovitz. 1999). Dromiciops gLiroides is (Caenolestid ae and Pichipilic1ae), small· to medium-size lhe only South American marsupial reported to exhibit deep inseclivore- fru givores (Palaeotb entidae), and small- to torpor or hibemation (Greer, 1966; Bozinovic el al., 2004). medium·size frugivores (AbdeliLidae). As yet only two speci· In the summer season thi s species is acti ve during the mens including postcrartial and cranial rem ai ns are reported ni ght, being a common mammal of the understory stratum for Pancituberculata (Abello and Candela, 2010). These were (Rodriguez-Cabal et al .. 2008) . referred (0 two palaeothentid species, Palaeothentes minu.ru.s The living Paucituberculata include fi ve species th at Ameghino, L887 and Paloeolhentes lemoinei Ameghino, are grouped in the genera Caeno/estes, Lestoros, and 1887 , from the late Early Miocene (Santa Cruz Fonnation). RhYllcholestes, all belonging 10 Caenolestidae ("shrew oppo· Curso-saltatorial locomotor srrategies were in ferred for both sum s"). This clade has a disjunct Andean distribution that species (Abello and Candela, 20 I 0). ranges from Venezuela Lo northern Pem (Caenolestes; In this chapter we summarize previous paleoecological Albuja and Patterson, 1996), central Pem and Bolivia studies of Sanl acrucian Paucituberculala, and present the (ustoros inca; Anderson , 1997; Ramirez er ol., 2(07) and results of a new paleoecological analysis of Santacrllcian southern Chile and Argen tin a (Rhyncholestes; Patterson and Microbiotheria. Additionally, we evaluate the paleoenviron Gallardo, 1987; Birney et aI. , 1996). Caeno1estids have a mental significance of non-carnivorous Miocene marsupials. wide latitudinal and al tirudinal (up to 4000 meters above sea level) di stribution . spanning several biomes including 10.2 Santacrucian pattcituberculatans Paramo, Montane foresl, and Valdi vian forest. Extant caeno and microbiotherians Ie..<;tids are small shrew·sized marsupials, which inh abit moist and dense vegetated microhabitaLs (Kirsh and WaJler, 1979; During the South American Miocene, paucituberculatans and Kelt el al., 1994). The scanty ecological data reported in the microbiotherians coexisted with other metalhelians such literature indicate that caenol estids have a cursorial-leaping as Sparassodonta , polydolopimorphian Argyrolagoidea, and locomotion, and a plimarily insecti vorous diet (Kirsh and Didelphimorphia. Paucituberculatans occur in most Miocene Waller, 1979; Barkley and Whitaker, 1984 , Patterson and assemblages, but Argy rolagidae and Didelphimorphia are rare GaiJardo, 1987; Patterson, 2007). or absent as is tbe c:'15e for the late Early Miocene fauna of Santa 158 Mana Aleiandra Abello et al. a b e n Fig, 10.2. Dentition of se lected Pauciluberculala and Mi crobiotheriidae species or the Sama Cruz Formation. a, b, Mic:rohiolherillrJ! acicIIlcl (MACN-A 5727) left. mandibular fragmen! with 1111-4 in labial (a) and occlusal (b) views. c, d. MicrohiothenllfJ1 gallegosl'l1se (Lype AMNH 9591) right mandibular fragment wilh p3- rn3 in lab ial (c) and occlusal (eI) views. e, f. Stifotherium dissimile ([ype MACN·A 8464) right mandibular fragment wit h i2 , i3 alveoJous, three one-roOfed teeth and p2-m4 in labial (e) and occlusal (f) views. g, h, PhOllocdromlls g/'acilis (lype MACN-A 8457). left mandibular fragment with p3-m3 in labial (g) and occlusal (h) views. i, j, Palaeolhenfes minutllS (MACN-A 5591-5518a), right malldibular fragment wilh p3- m4 in labial (i) and occlusal (j) views. k,), Acdesfil' owenii (type 11ACN ~ A 1379) mandibular fragment wi th i2, fonr alveoli of one·rooted teeth, complete p3-m 1 and m2 trigonid in labial (k) and occJu!>al (I) views. In , n. Abderites meridionalis. (01) (MLP 55· XIl·13-145) mandibular fragment wilh iI, four alveolous of one·rooled teeth and p3- 01 1 in labial view, (n) (Lype MACN·A 12) mandibular fra gment with T);lI - 3 and m4 alveolous in occlusal view. Scale bar, 2 mm. Cruz beds. To date, mi crobioth eri ans (Fig. 10.2a- d) and Institutional abbreviations paucituberculatans (Figs. lO.2 e- n and 10 .3) are the only MACN , Museo Argentino de Ciencias Naturales non-carnivorous merarherians recorded in rhe Santa Cmz "B. Rivadavia," Buenos Aires, Argenrina. MACN-A, Formation. Metarherian s of this formation were first Colecci6n Nacional Ameghino. descri bed by Ameghino (1887, 1891). Sinclair ( 1906) and MLP, Museo de La Plata, La Plata, Argentin a. Marshall (1976a, 1980, 1982) made significant contribu AMNH, American Museum of Natural History, New tions to the knowledge of the di ve rsit y of Sanfacrucian York, EEUU. pauc iru bercularans and mi crobiolheriids. Recent revisions MPM-PY, Museo Regional Provincial Padre Manuel include those of Bo wn and Fleagle ( 1993), Tauber (1997), Jesus Molina. RIO Gallegos, Argentina. Abello (2007), and Abello and Rlibilar-Rogers (in press). An updated ta xonomic li st and the records of pauc itu ber 10.3.2 Melbodology cul alans and microbiotheriids from localities of the Santa To estimate body masses and infer dietary preterences of Cru z Formation are presented in Appendi x 10. 1. SantacllJcian non -camivorous marsupials, we fo ll ow the methodologies of Dumont er al. (2000). In (he context of an analysis of dietary preferences of Paucirubercul"ta, Dumont el al. (2000) studied all available Santacrucian species. Here 10.3 Materials and methods we summari ze the results of these dietary reconstructions, and The mareJi al studied is li sted in Append ix 10.2. apply the same rnethcxlalogy to [he Sancac[1Jcian Micro biotheriidae. In contrast to Dumont et al. (2000), we follov. 10.3.1 Abb,.eviations Abello and Rubilar-Rogers (in press) in considering The generalized metatherian dental formula is: IIi 5/4, C/c A. mer;dionalis Ameghino, 1887 La be a different spec ie 5i 1/1. Pip 3/3. M/m 4/4. from the Colhuehuapian Ahderite.\· crisplls Ameghina. 1902. Paleoecology of Santacrucian Paucituberculata and Microbiofheria 159 Ru d b Ft It f 9 Mm Latf Tt ff~: Anf m k n Fig. 10.3. Postcranial skeleton of Pa/aeothentcs species. Pa/acofhenres minutus: a, b, right humerus (MACN-A 56 I 9-5639c) in anterior (a) and posterior (b) views; c, d, right ulna (MACN-A 5619-563ge) in lateral (c) and anterior (d) views. e, f, Right radius (MACN-A 56 I 9-5639d) in proximal (e) and medial (f) views. g, Pelvis (MACN-A 5619-5639f) in lateral view: h, right femur (MACN-A 56 I 9-5639g) in anterior view: i, left femur (MACN-A 5619-5639h) in anterior view. Pa/aeOlhelltes /emoinei (MPM-PV 3494): j, k, left tibia in anterior U) and lateral (k) views; I, right tibia in distal view; m, right asrragalus in dorsal view. PaiaeOlhenies minUius (MACN-A 5619-5639i); n, right calcaneum in dorsal view. Scale bar, 4 mm. Abbreviations: A. acetabulum; Aff, astragalofibular facet; Auf, astragalouavicular facet; Atc, anterIor tibial crest; Bt, bicipital tuberosity: C, capitulum; Cacud, cuboid facet distal half; Dc, delLopectoral crest; Ef, ectal facet; Ft, femoral tubercle; Gt, great. trochanter; It, ischial tuberosity; Latf, lateral astragalmibial facet; Lec, lateral epicondylar crest; Lt, lesser trochanter; Matf. medial astragalotibial facet; Me, medial epicondyle: Mm, medial mallcolus; Of, olecranon fossa: Op, olecranon process; Pt, peroneal tubercle; Pte, proximal trochlear crest; Raf, radial articular faceL for t.he capitulum; Ru, radio-ulnar facet; Sc, supracondyloid crest; Sfa, sustentacular facet; Sfo, supracondyloid foramen; Srf, supratrochlear foramen: T, trochlea; Tn, trochlear notch; Tpe, ribial posterior extension; Tl, third trochanLer. 160 M ar/a Alejandra Ahello el al. Regardi.ng the locomotor habits of Palaevchente.s species, Labial we present here a synthesis of Abell o and Candela's (2010) main results. Body mass Body masses were esrimated from the Anterior occlusal area (mes iodisLal length x lab iolinguaJ breadth) L of the second lower molar, usin g the linear regression equation In bod y mass = 2.4 19 + ( 1. 727 x In 111 2 area) (Eq . 10.1) deri ved by Dumont el al. (2000) for li ving marsupials. T hi s equation included 27 extant marsupial species whose body masses range from approximately 10 10 1500g, <.I wide Fig. lOA. Occlusal view of lert lower second molar showing lhe range encompassing that of Sanl3cI1Jcian marsupi als. shearing cresls 1-6 (Kay and Hiiemac. 1974) measured in Ihi s study. Locomotion and use of the substrate To assess the loco motor strategies of Palaeo/hemes minutus and P. /emoinei, (SRA) is the SUul or length . or crests l-u di vi ded by the A bell o and Candela (2010) performed a 1ll0lJ>hofunctionai square root of tooth area, i.lnd the shearing ratio based on analysis based on comparisons with living South American length (SRL) is the sum of lengths of crests I-u divided by marsupials. molar length. PalaeOlhenles minUlus (MACN-A 56 19- 5639a-i) is the The present analysis is based on those performed most iUlportant specimen available, being represented by by Dumont el al. (2000) for paucituberculatans, who the humeros, radius, ulna, femur, pelvis, and calcaneum included the following living marsupials as models: four (Fig. lOJa- i, n). The postcranium of P. lemoinei (MPM-PY insectivores (the p~lU citub e r c ul Table 10.1. Body mass es timates and diet of Santacrucian M icrobiotheriidae and Paucituberclllata 2 Sample size m2 area (mm ) Body mass Diet Microbiotheria Mi crobiolherii dae Microbiolherium acicflla 138 20 g [nsectivorous M icrobiorherium patagolliCLlJl1 2.07 40g Insecti vorous Microbiorherium fehuelchum 2.66 6 1 g Insectivorous M icrobiofherilln/ gal/egoSeJ1se 4.44 147 g I nsecti vo rou s- frugivorous Paucituberculata Caenolesrid ae SliLOlheriurn dissimile 3 1.48 37 g In secti vo rou s- frug ivorous Pi chipilidae Phon.ocdromus gracilis 2 1.04 28 g lnsecti vorou s PalaeO lh entidae Pa/acOlhentes aratae 13 11.34 860 g Fru givorous Paiaeorhellles min.u!us 112 3.06 82 g Insecrivorou s Pa/acorhclues intern/edius 30 4.67 192 g Insec ri vorous Pa/aeor i1 etlfes lemoin ei 28 7.18 425 g In sectiv orous PaiaeOlhellles pas{,'uali 6 2.25 38 g In secti vorous Acdeslis owen£; II3 6.7 1 344g Frugivorous Acdes/is Icmairei 18 S. 13 256 g Insecti vorous-fiu gi vorous Abderilidae Abderiles merid£onalis IS 8.86 487 g Frugivorous 2 The sample size and mean m2 area (mm ) from which the bod y mass was reconstructed are presented. Inferred diet (Diet) is based on shearing rat io and body mass data. 162 Mar/a Alejandro Abello et a!. such as CQenolestesfuliginosus and Metachirus nudicaudalus 10.4.3 Feeding habits (Abello and Candela, 2010). Characteristics of the forelimbs Plots of SRL and SRA show the separation between extinct include, among other features, a deep and high humeral and extant frugivorous and insectivorous speCIes trochlea (Fig. 10.3a), a deep olecranon fossa (Fig. JO.3b), (Fig. 10.5). Both ralios indicate that most extinct micro and mediolaterally broad proximal trochlear crest (Fig. biotheriids were insectivorous. Microbiotherium acicula is lO.3c, d). These featmes indicate a well-stabilized elbow the microbiotheriid with the highest SRA and SRL joint. The short lateral epicondylar crest (Fig. 10.3b) and the values, equaling the living insectivorous Caenolestes suboval radial head (Fig. lO.3e) suggest that pronation-supin caniventer and Sminthopsis crassieaudata 10 SRA ation was limited (Abello and Candela. 2010: 1520). The ratio. The SRL value of Microbiotherium patagonicum is pelvis, better preserved in P. minutus, shows a restrictive close to that estimated for Dromiciops gliroides, while acetabulum (i.e. tightly articulating; Szalay and Sargis, M. tehuelchum and M. gallegosense present lesser SRL 2001), lengthened ischium, and prominent femoral tubercle values than D. gliroides and M. aeicula, indicating a less as well as ischial ruberosity (Fig. 1O.3g). The morphology of shearing development in these species. Microbiotheriurn the pelvis indicates a high stability at the ilio-femoral joint gallegosense has an SRA value comparable to those of and an increased mechanical advantage of the flexors and the living Australian frugivores Petaurus breviceps and extensors of the hip (i.e. rectus femoris and hamstring Acrobates pygmaeus. However, M. gal/egosense clusters muscles), which are well developed in saltatorial species with the modern insect.ivores based on SRL ratio (Argot, 2003a). The greater trochanter of the femur projects (Fig. 1O.Sb) beyond the proximal surface of the femoral head (Fig. 10.3i), Among pauciluberculatans, three species (Abderites indicating that the gluteal muscles were favorably positioned meridionalis, Aedestis owenn Ameghino, 1887, and to produce fast extension at the hip joint, as occms in agile Palaeothentes aratae Ameghino, 1887) cluster with modem and leaping species. Additionally, the hind limbs of frugivores on the basis of SRA and SRL ratios. Conversely, Palaeothentes species, like those of curso-saltatorial f0I111s, Phonocdromus gracilis Ameghino, 1894 (Fig. 10.2g, h) and have features associated with marked stability for flexion and the palaeothentids Palaeothentes pascuali Bown and Flea extension in the parasagittal plane. Among these functionally gle, 1993, P. minutus, P. intermedius Ameghino, 1887, and significant traits are the right angle betvleen the medial and P. lemoinei cluster with the living insectivores. Finally, the lateral astragalotibial facets at the cruroastragalar joint caenolestid Stifotherium dissimife (Fig. 1O.2e, f) and the (Fig. 10.31, m), and the conformation of the transverse tarsal palaeo then tid Aedestis lemairei are classified as frugivorous joint, characterized by tbe distal and prox.imal calcaneo or insectivorous depending on shearing ratio (i.e. as insect cuboid facet forming a right angle (Fig. 1O.3n). ivore-frugivore, Fig. 10.5a, b). (a) Fig. 10.5. Partition be[ween frugivorous and insecLivorous Laxa (b) Frugivores Insectivores based on SRA (a) and SRL (b) ratios. Paucituberculatans (crosses). Frugivores Insectivores petaurids (filled circles), dasyurids (open circles). microbiotherids (diamonds). Specie:'. are: I, Sfilothl'rium dissimile; +1 +2 2, Phonocdromus gracilis; 3, Ahderites meridionalis; 4, Acdestis +2 3+ owenii; 5, Acdestis lemairei; 6, Palaeothentes millutlls: 3+ 7, PalaeO/henle.1 pascuafi; 8, Palaeolhellres ;nlermedius; 4+ 4+ 5 5 9, Pafaearhenfes lemaine;; to, Palaeorherlres aralae; 11, LestQros +6 +6 inca; 12. eaenolestes coni Fenter; 13, An{echinus stuartii; +7 +7 14, Sminl.hopsis crassicaufialO; 15, Petaurus breviceps; +8 +8 16, AU'obates pygmaells; 17, Dromiciops g/iroides; +9 9 18, Micro/JiorheriulrI acicula; 19, Microbiotherillm po/agon;cum: 10 + 11 + 12 20, MicrohiorheriunI galiegosellse; and 21, Microbiorherium + 11 + 12 + tehLle/chum. 13 e13 .14 15 0 e14 160 15 .17 160 .17 .18 .18 .19 20. 19 20. .21 • .21 2.00 2.50 3.00 3.50 1.50 2.00 2.50 3.00 SRA ratio SRL ratio Paleoecology oj Somacrucian Paucifuberculara and Microbiorheria 163 10.5 Discussion , ._._- 10.5.1 Body mass 700 , In a study of extant Neotropical marsupials, Birney and 600 , Monjeau (2003) analyzed the distribution of bod y size among species and established three size categori es: (a) 500 , small-sized (less than 100 g): (b) medium-sized (from 100 <0O9 to 499 g); and (c) large-sized (500 g or more). Taking into ,.. 300 9 account these size categories, we found th at Santacrucian _... microbiOlheriids were mainly small -sized, wit.h estimated 200 , ,.., - body masses ranging from 20 g in MicrobiOlherium acicula "0 , to l47 g in M. gallegosense (Fig. lO.2c, d). Santac rucian _ ~ . fl pauciluberculatans show a much greater body-mass range, ! •~ • extending from l3 g in PhoJl ocdromus gracilis to 800 g in t a •l! j Paloeothemes aratae, and with more than half of the " ~a " ~ species being small- to medium-sized (Table 10,1). a • " Throughout the Cenozoic, most South Ameri can meta OCO ' ~------I~- -; therians were small- to medium-sized (see Goin, 2003). In "0' ------.....-.------.- extant fauuas, smaU- to medium-sized marsupials represent - about 90% of the marsupial faun a of the Americas (see 6OO0 ~------4rf__1 Birney and Monjeau, 2003), and they are also abundant in ~ , ~------_...~f__1 the marsupial fauna of Australas ia (Dickman and Vieira, 2006). Our results are in agreement with this pattern, . oog ~------f~f_~1 because 52 % of the Santaclllcian marsupia! species are WO, ~------p~ ---~4ri_~1 small- to mediurn- s i ~ed (nine paucitubercul atans plus four 200 ~ ~------microbiotherLan species; see Table 10.1), and 48% are large (one paucituberculatan species plus II sparassodon( 1 0 0 ~ ~------~-~ ---_F.~i_~1 species; see Table 10.1 and Prevosti ef aI., Chapter 11 ). I Sanracrucian paucitubecculatans and microbiotheriids j i show a body mass overlap in the small and medium size ~, Q categories (Fig. 10.6a, c). Ne vertheless, the differential use .~ of space and food resources may have miuimized or avoided competition among spec ies of similar body mass, as in b ~ extant marsupial ct ssemblages (CharleS-Dominique e! 01., ,OO, ~------1 198 1; Charles-Domiuique, 1983: Vtetra and Monteiro-Filho, 2003). , oo , ~------I ~,~------l 10-5_2 Locomotion and use of the substrate 5 00' ~------__1 Locomotor strategies constitute an imporLant dimension of a .OO 9~------_1 species' ni che. For extinct mam mals, locomotion may be inferred from fossil postcranial remain s, and have implica 3 00 '~------_1 tions for species paleoecology. Unfortunately, only Iwo ~, ~------~------~ skeletons of non-carni vorous Santacrucian marsupi als are 100 Q ••...•_ . ______---.-.. ------ known. Both skeletons (pertaining to two diffe rent palaeothentid spe<.: ies) were recentl y analyzed by Abell o and Candela (2010) who paid particular attention to the reconstruction of locomotor pattern . As noted earlier, in lenns of fun ctionally significam features, Ihe major similar c ities were found with the extant mars up ials Caenolesfes ju/iginosus and Meta(."hirus nudicaudofus. The latter is the Fig. 10.6. Body mass averages of insecri vorous (a), frugivorou s (b), and inse c tiv o r ou.~-rru g i vo ro u s (c) non -camivorollS marsupi als of most terrestrial di de lphid (Miles el af., 198 1; Delciellos and Santa CruL Formal.i on. Gray bars: pauei.tubercul utans; black bars: Vieira, 2006, 2009). This ma rsupial inhabits a wide range of microbiotherjids. Values fro m Table 10.1. forest habitats (Miranda el of., 2009), from open scrub 164 Maria Alejandro Abello et al. vegetation (M il es ef at., (981) to lowland and hillside According (Q our results. Miocene microbiotheJiids als o woodlands (Moraes, 2004). In th e wild it was observed were mainly insec t.i vores. Only one s ~ c ies, M . gaJlegosense, bonnding on the ground, swift.ly negoti ating obstacles at has shearing wtios that indicate a more limited shearing high speed (Miles el 01., 198 J). Caenofesles species occur component, suggesting an inse ctivorous-frugivorous diet in the Andean highlands biomes such as Montane and (Fig. 10.5a, b). Microbiotherium acicula is tile most exLreme e land forest<;, and Paramo. In these biomes caenolestids in sectivorous species, showing the highest SRL and SRA inhabit forests with or without dense undergrowth , and the values. Microbiotherium palaROnicum is closer to the extant grassland- forest ecotone (Ki rsh and Waller, 1979; Albuja Dromiciops giiroides in SRL va lues, aud it achieved a similar and Patterson, 1996). Coeno/estes and its relative Lestoros degree of molar crest developme ut as in the living species. cau leap at high speed usi ng anteri or and posterior limbs In our analysis, D. gliroides is gro uped wi th insecti vorous simultaneously (Kirsh and Waller, 1979), species (Fig, 10.5a, b). This resu lt is consistent with the Locomotor behaviors of M. nudicaudatus and caenoles information of its main dietary prefe rences in the wild. lids have clear anatomical correlates in their poslcraniai Analys is of stomach contenrs indicated that thi s species skeletons (Grand, 1983; Argot, 2003a. b), a particularly feeds primarily on arlhropods and other in veltebrates importan l aspect for functi onal int etpretations in fossil (Mann , 1955; Meserve et 01., 1988). However, it also feeds species. Pa faeoth entes speci es exhi bit en hanced joint sta seasonall y on fruits (Amico ef af. , 2009) . Thi s strategy bility and parasagittal movement (Abello and Candela, could be extrapolated to SanLacJlJcian microbiotherijds, as 2010). Additiona ll y, features associated with fa st move insectivores may consume plant material, either regul arl y or ments and leaping have been identified. In conclusion, seasonally, when prey species are scarce or un avail able P. minutus and P. lemoinei were probably agile species with (Hume, 2003). running and leaping abilities re sembling Caenolestes, According to molar crown morphOlogy, Miocene Lesforos, and Merachirus. paucituberculatans were considered insecti vores, insect Even though the locomotor strategies described by AbeHu ivores-frug ivores, and insecti vores- ph ytophages (e.g. and Candela (20 I 0) were established for only two Ortiz-Jauregui zar, 2003). Our analys is corroborates this Palaeorhenles species, il may be speculaled th at other species inference, showing that in sec(j vores are more di verse of the genus, such as P. pascua/i and P. i.11lermedius, may (five species) than insectivore- frugivores and frugivores have had similar locomofor abilities. In ilddition, it is possible (induding the insecti vorous-phytophagous category of that scansorial or arboreal locomotor behaviors evolved Orti z-Jauregui"r, 2003; see above) (Table 10.1). As among non-camivorous Santacruciall marsupiaLs. Dumont et af. (2000) pointed out, folivory seems not to We note that. the ecological dive rsity o[ nOll-carui vorons have evolved in pauci rn berculatans, as no taxon with hi gh Santacru cian marsupials evaluated here is simil ar to thal of shearin g ratios has an estimated body mass higher than CU 1Tent tropical habitats of South America (see below). In 600 g (S mith and Lee, 1984). extant ecosyslems) ecological diversity is positively correl Most insecti vorous paucittlbercul atans di ffer markedl y ated with habitat complexity (i.e. with the development of in body ma'>S (e.g. Palaeoth entes millu{us, P. intermedius, vert ical strata in a habitat; August, 1983). In the case of and P. lenlO;nei), suggesting that ecological separation Santacrucian marsupials, the ecological diversity inferred among them may have been achi eved by differences in here would seem to reflect a ve rtical heterogeneity. In this dietary composi tion and/or consumption of prey of different comext, it is possible to infer that [he vertical space of these body size. In living in secti vores, such as dasyuri d marsu habi tats could be exploi ted by Santacrucian marsupials pi als and soricid piacentaLs, there is a positive cOlTelalion through scansorial and/or arboreal habits. Vertical space between body size of predators and their prey (Fisher and offers an additional dimension for niche partitioning, and Dickman, 1993; ChLlrchfield e/ aI., 1999). Even so, both hence the possibility of more species coexisting in the same small and large dasyurids can exploit a relatively large area (Mi les et al., 198 I ; Vieira and Monteiro-Filho, 2003; range of prey sizes, and there is no ph ys ical constraint on Croft and Eisenberg, 2006 and refe rences therein). the size of prey consumed. Consequentl y, dasyurid species max imized their rates of energy intake by feeding on prey 10.5.3 Feeding habits of a selected size (Fisher and Dickman, 1993). Thus, larger According to the cro wn morphology of its molars, Miocene dasyurids prefer larger invertebrates be cause of greater microbiotheri ids were considered insectivores or in sec( energy return per prey item; conversely, for {he smaller ivores/frugivores (Pascual and Bond , 1986; Goin, 1997). dasyurids prey consumption requires more chewing time, Based on an analysis of molar wear facels. Goin e! al. (jn and this could resull in a fall in the rale of energy intake press) concluded th at Ea rl y Oligocene Patagoni an members from eacb prey (Fisher "nd Di ckman, 1993). Despite small of thi s family (inclu ding Microhiotherium , Fig. 10.7. Life reconstructions. a, Abderitcs meridlonalis and b, Palacothcl7f('S minu/lls. Drawing by Pablo Motta. percentage of several invertebrate prey in the diet (Church pJesiadapifoffil primates (e.g. CaJpodaptes Matthew and fie ld ef 01., 1999). We expect th at dietary composition (as it Granger, 1921). In the 1l1ultituberculates and plesiadapi covaries with body size) would have produced niche separ forms, the shearing teeth mainly exhibit apical wear, because ation among extinct insectivorous paucituberculatans. the lower cutting teetb become wom when the food is ground As mentioned above, the body mass of Santacrucian against a cllspate upper tooth. In contrast, in Phalanger, and microbiotheriids and paucituberculatans overlaps to some probably also in Abderites, the food items are Cllt between the degree in the .small to medium size range (Fig. 10.6a), upper and lower teeth as they shear across one anotber in a initiall y suggesting th at some niche overlap may have scissor-like fashion (Dumont et al., 2(00). A shearing com occurred. Howeve r, differences in body size and molar plex .s imilar to that of the abderitids occurs in many extant morphology suggest that niche ove rl ap was, in fact, min Diprot.odont.a, including thc Phalanger already men tioned as imal, and it is also possible that differences occurred not well as Burramys and the Potoroidae HypsiprymnodolJ and only in diet composition, but also in foraging mode (San Bettongia. Related to their fun cti on, these denial modifica son, 1985; Churchfi eld and Shefrel, 1994; Church fi eld tions arc adequate to bJ(:ak open food items with a hard el al. , 1999). covering (Dimpel and Calaby, 1972; Parker. 1973). Fmgivorous and insectivorous- fru givorous marsupials On the othcr hand . Palaeolhentes ara/ae and Acdestis analyzed here do Ilot exhibit body mass overlap (compare owenii have a strong shearing crest (paracri sta) ou m I Fig. 1O.6b wi dl IO.6c). Frugivorous species are paucitu ber (Fig. 10.2k, I), but they lack a plagiaulacoid dentition and cul atans belonging to Palaeothen(idae (PalaeOfhenles ora/ae lophs. These differences suggest that fru givorous paucitu and Acdestis owenii. Fig. 1O.2k, l) and Abderitidae (Abderites herculatans were distinct not only in body mass but in their meridiOllolis. Figs. IO.2 m, n and 10.7a), which are quile diets as we ll (Ortiz-Jaureguizar, 2003). di Slincl in dent al morphology (Abello, 2(07). The dent il ion of Abderitidae is characleJ; zed by the presence of well 10.5.4 Paleoenvironmental implications developed lophs and a plagiaulacoid compl ex (S impson, From thc wide range of estimated body masses and diet of 1933; Ort.iz-Jaureguiz3r, 2003). The pl agiaul acoid complex non-carni vorous Santacrucian marsupi als, several ecologic of Abderiles was considered by Dumont el al. (2000) a" a niches were reconstructed: smaJl- (0 medium -sized insect dieta lY indicator in addi tion to body mass and extent of molar ivores, and small to large frugi vores and insecti vores shearing. According to their analysis, occlu sion between P3 fru givores. In regard Lo a paleoecological reconstruction, and ml in Abderite!'· was a shearing complex that operated in this ecological diversity suggests the existence of foresled a manner sim ilar to that of hving Australian phalangerids ha bitats that couid have sUpp0l1ed the diverse marsupial such as Phalanger, but di ssimilar to those of other mammals niches. in modem ecosystems, and particul arl y in tropical with pJagiauJacoid dentition such as certain Cretaceous 1.0 forests , high values of mammalian species richness arise Early Eocene multituberculates (e.g. the cimolodontan from habitat heterogencity. mainly owing to the pa11itioned Plilodus Cope, 1881 ) and North American Paleocene vertical space (Augusl, 1983; Bakker and Kell, 2000). 166 Mana Alejan.dro Abello et al. Species richness also tracks plant prodncri vity, with higher in forested habirats developed under warm temperatures and productivity leading ' 0 more species (Kay el aI., 1997). rain seasonality. According to rhe fossil record of vascular Paleoenvironmental inferences can also be advanced by plants, the distribution of megathennal and mesothennal analyzing the trophic guild slrUCl11re of Santacrucian mar angiosperms expanded their distribution at middle-high supials. In a macroec.:ologicai stu dy of Neotropical marsu latitudes of Patagonia during the Late Oligocene to Early pials, Birney and Monjeau (2003) evaluated the latitudinal Miocene (Barreda and Palazzesi. 2007; Brea et at., ChapLer variation among several biological characters, such as 7). Neveltheless, the first records of some shrubby and trophic guild structure. habitat use, and body size. Taking herbaceous angiosperms in sou thern South America suggest into account that latitude is a surrogate fo r physical environ that the vegetation acquired a more complex physiognomy mental variables sucb as temperature and precipitation, the than that of the Early O li gocene (Barreda and Palazzesi, trophic guild structure of Santacrucian marsllpials may offer 2007). During the Early Mi ocene, xerophytic (or mesophy clues to the Santacrucian paleoenvironments. According to tic) vascular plants were dominant in Patagonia, and the Birney and Monjeau (2003), three guilds were considered: development of all these speci£llized communities was prob frugivores. carnivores. and in secti vores. Current carnivor ably related to a water deficit in open forest regions or ous marsupials include, among othe rs, the didelphids marginal marine areas. Durin g the late Early Miocene, Didelphis, LUfJ'eolino. and Philander, all of them having rainforest trees may have formed ripari an or gallery forests body masses less lhan 2 kg. In the S<:t ntacruc ian assemblage. in central Patagonia, while drie r conditions would have call1i vores with body masses less than or equal to 2 kg prevail ed in lowl£l nd areas (Barreda and Palazzesi, 2007). include the sparassodonts Sipa/ocyon gracilis Ameghino, Finally, during the latest. Earl y Miocene , xerophytic elem S. obusfa Ameghino, Pselldol1O!iClis plisillus Ameghino, ent s suffered a geographic retraction in Patagonia, with an and Perarhereures pU118ens Ameghino (see Prevosti e! al., increase of megathelmals and a dominance of aquatic he rbs Chapter I I). Thus, smaJt carni vores represent 22% of the and hydrophytes. Forests persisted across extra-A ndean Sanracrucian marsupia l species richness, insectivore-frugi Patagonia until about the Middle Miocene (BalTeda, 2002; vores plus frugivores 33%, and insectivores 45%. Compar BaITeda and Palazzesi, 2007; Palazzesi and Barreda, 2007). ing the trophic guil d structure of Santacrucian marsupials If we consider the ecological infonnation provided by al l with those of the modern Neol-ropics, we find that in the the Santacrucian mammals (Prevosti el al., Chapter 11; Santacrucian fauna there is year-long avail ability of fmits, and the percentage of Pa.sc ual er aI., 1996; Orti z-Jauregui zar and Cladera, 2006, frugivores is higher lhan at hi gh latitudes. Additionall y, and refe re nces therein). From a climatic point of view, the differences in precipitati on (i.e. seasonaJ ra infa ll) seem [ 0 presence of primates and othe r walm c1imare -sensiti ve ver be anothe r importa nt factor influe nc ing the abundance of te brates tha t have been recorded as far south as 5 1°S sug frugivores (Bimey and Monjeau, 2003). If we consider this gests that wann and forested habitats were well developed last factor, the sharp differences between dry and wet in Patagoni a. Nevertheless, together wi th these indicators of season ~ in the tropics would have all owed more diversifi waJm and forested habitats, there were also other mammals calion in the trophic niche than more constant precipitation. such as some rodents that indicate the existence of open On the basis on these ecological similarities, we can infer habitats encroaching on areas of wet forests in Patagonia that Santacl1lcian marsupia ls lived in relatively wann cli (Pascual el 0/., 1996 ; Ortiz-Jaureguizar and Cladera, 2006; mates, bUl with seasonal rainfall. However, it should he kept Perez. 2010). in mind that taphonomic bias and time averaging are Considering the evidence provided by vascular plants and common fac tors that affect the composition of fossil assem mammals, we may conclude that the ecological diversity of blages. Consequently, in th e absence of a precise evaluation the Sant£lcrucian marsupials is compatible with the exisl of the incidence of these biases, the infereuces derived from ence of habitat patchiness during Santacrucian times, with a a fossil assemblage have a less heuristic value that those balance between closed and open habitats represented by u based on living assemblages. park savanna. In this scenario, the non-camivorous marsu In summary. the ecological charac.;teristics of non-c.;arniv pial species would have occupied the more forested area~ orous marsupials of the Santacrucian suggest that they lived (Fig. 10.7). 167 Paleoecology of Sa11lacrucian Paucilftberculata Gnd Microhiolheria 10.6 Conclusions From the present study, lhe ecological diversity of the non-camivorous Santacfll cian marsupi al indicates IJ1 al rhey Microbiorheria and Pallcitubercul ata of the Santa Cruz lived in forested habitats, under wanT} temperatures aud rai n Fonnation constirute an ecologicall y diverse assemblage seasonality. Forested habitats coul d have supported rhe of non-carnivorous mar,;;upiats. Among microbiotheriids we varied pr eviollsly menrioued mar:) upial ni ches, offering recoouize small insectivores such as MicroiJiorherium diverse resources ;n the spatial and Irophic dimensions. c acieliia and M. tehuelclwm, and a medium-sized insect Considering also the paleoecologic<:t l iuformation provided ivore- fru givore, M. ga/legosel1se. Compared with micro by vascu lar plants and al l the mammalian species, we con biotheriids, pauci ru bercuJ alans are taxonomicall y and clude rhat the ecological di versity of non-carnivorous mar ecologicall y more di verse, hav in g a wider range or body supi als is compatible with a patchy environment, with a mass and diet. For rhi s group we jdentify small ill ~c tivores balance between vegerati on typical of closed and open such as PhOl1ocdrO l11lf S gracilis. medium -sized curso-salta habitats, represented by a park savanna. torial insecti vores such as PaJaeolhellles mintllUS (Fig. 1O.7b) and P. lemoinei, the small- to medium-sized inseclivores fl1Jg i ores Stilotherium di.ssimile and Aedes/is owenii, the v ACKNOW LE DG M EN T S medium-sized frugivore Abderite::; meridiona/is (Fig. 10.7a). We thank D. Flores (MACN), A. Kramarz (MACN), and and rhe large fl1J givore Palaeofhemes amtae. M. Reguero (MLP) for facilitating access to specimens of Regarding the marsupials of the insectivore gu ild, a min marsupials in their care, and F. Goin (MLP) for aJlowing us imal niche overl ap was inferred from differences in body to srudy speci mens in his personal co ll ecti on . Special mass and its relations 10 prey size and diet composition, as thanks 10 rhe ed;[Qrs of Ihis volume, S. F. VizcaIno, is observed in extant in secti vorous mammals. ]n add ition (0 R. F. Kay, and M. S. Bargo, for inviting uS to make this the inferred terresrri al , curso-salta[Qria l locomotion of cont ribution, and 10 P. Posadas (LASBE·MLP) and Palaeothellfes m;l1u/us and P. lemoil1ei, scansori al or arbor C. Morgan for their help with the English version. Thi s is eal locomotor behav iors could have evolved among non a contri bution to the projects PICT 0 143 to Sergio carnivorous San lacrucian marsupials that allowed their F. Vizcaino and NSF 085 1272. 0824546 to Richard F.. Kay. ex ploitation of resources in the venical space. Appendix 10.1 Paucituberculata and Microbiotheria of the Santa Cruz Formation Microbiolheria Ameghino, 1889 Monte Leon (Col. Bown and Fleagle): Palaeolhenles ararae. Palaeolhemes minl/tlJ..'I, Palaeothenles intermedius, Microbiothe riidae Ameghino, 1887 Palaeothentes !emoinei, Aedesti,t owenii, Aedes/is lemairei, Microbiotheriwll acicula (Ameg hino. 189 1) La Cueva (Col. Ameghino): Phonocdromus gracilis, Microbiolheriu.m patagoniulln A meghino, 1887 Polaeothemes minUlus, Poloeorhentes intermedius, Microbiorherium teliue/chum Ameghino, 1887 Polaeofhenres lemoinei, Stilofherilll11 dissimile. Ahderifes Microbiorheriul7I ga//egosense Sinclair, 1906 meridiOl/olis, Microhiotherium pafOgonicllm, M icrobiother illm te/I/Je lchwn. PaucitubcrcuLata Ameghino, 1894 Yegua QueOlada (Col. Ameghino): Palaeofhenles interme Caenolestidae Trouessart, 1898 dius, Palaeothcntes lemoinei, MicroiJiolherillfrl tehue!chwn. Srilolheriun1 dissimile Ameghino, 1887 Saota Cruz (CoL Ameghino): Pa/aeOlhcn fes aratae. Pichipilidae (Marshall , 1980) Palaeolhenles min.ufus. Palaeollientes lemoinei, Micro Phollocdromus gracilis Ameghino, 1894 biolherium pOlagoniclim. Palaeothe ntidae Si nclair, J906 Monte Observacion (= Ceno ObservalOrio. see Marshall, Palaeorhel1les oratae Ameghino, J887 1976b, and Vizcaino el al., Chap.er I; Col. Ameghino, Palacothentes minutus Ameghino, 1887 Bown and Fleagle): Palaeolhentes aralDe, Pa/aeothentes PalaeOlhenles intermedius Ameghino, 1887 minulUs, Palacolhentes pascuali. Palaeof/Jcmes intermedius, Palaeo/hemes lemoinei Ameghino. 1887 PalaeOlhenres lemoinei, S'tiloth eriwn dissimile, Abderi!es Palaeoth cmes pascuali Bown and Fleagle, 1993 merirlionaiis, Acrlestis Olrenii, Acdestis /emairei, Aedestis owenii Ameghino, 1887 Microbiofheriul11 acicli/a, Microbio/he/·fum patagoniclIIn. Acdesris lemaird Bown and F1eagJe, 1993 Micl"obiothel'iul11 lehuelchurn. Abderi.idae (Ameghino, 1889) Puesto Estaucia La Costa (= Corri guen-Aike; Col. MLP Abderites meridiollali.\ Ameghino, 1887 Duke Uni versity): Palaeolhenles lemoinei, Corri guen-Kaik (Col. Amegh.ino): PalaeOlhe!1les lemoinet, List of PoucililberclIlata and Microbiothaio from localities Microbiotherium tehuelehwn. of the Santa Cruz Formation KilIik-Aike (Col. H. Felton): Polaeothentes minutus. For details of the specimens. localities, data of collection Microbiorheriun1 tehue/chum. and collec.ors (Col.) see Marshall (1980, 1982), Bown and Rio Gallegos (Col. B. Brown): PolOeOlhel1les aralae. Fleagle (1993) and Vizcaino el 01. (Chap.er I: Figs. 1.1 and Paiaeolhentes minu/us. 1.2, and Appendix l.l). Near Feltou's Estaucia, along the uorth bank of the RIo Gobernador Gregores: Acdesris owenii. Gallegos (Col. Bamum Brown): Phonocd}"()fllus gracili.'i.. Lago Cardiel: Aedestis owenii, Microbiotheriwn adeula, Microbiorherium gallegosense, Rio C haJia - Ea. Viven Aike - (Col. Bown y R eagle): Sehuen (= Rio Cllalia; Col. Ameghino): Palaeolhentc> PaLaeothentes minulus, Palaeoff1enres imermedills, aratae, Palaeofhellfes !emoinei, Palaeothenles intermedill\, Aedestis owenii, Aedestis lemairei. Sri/otherilllll dissimile. AbderifeJ meridionalis, Micra- biOff1erium patagonicllm. 168 Appendix 10.2 Material studied Microbiotheriidae Palacothclllcs minutus M icrobiofherillrn acicula (Arneghino. 189 1), MACN-A 56 19-5639a- l, right and left mandibular rami MACN-A 5727, a left mandibulm ramus with p3-m4. with m3-4, di slal porti on of right humerus, proximal Horizon and locality: Santa Cruz Formation, Monte Obser portion of right ulna, parti a ll y complete pelvis, proximal vaci6n, Santa Cruz Province. ponion of right fe mur, proximal portion of left femur, and MicrohiOlherium palagonicIII1l Amegh illo, J887 right calcaneum . Ho ri zon and locality: Santa Cruz Forma MLP 11-30, a ri ght mandibular ramus with In 1-4. Horizon Lion , Killik-Aike, Santa Cru z Prov ince. and locality: Srulta Cruz Formation, collected from «las barrancos del no Sail/a Cruz" (A meghin o. 1889: 264). Palaeolhentes lemoinei Sant a Cru z Province. MPM-PV 3494. ri ght mandi bu lar fragment wlth m2-4 and MicrobiOlherium felwe/chum Ameghino, 188 7 left edentulous mandibular fragment, left humerus, left MLP 11-36, a right mandibulru" ramus with p2- m4. Hori ulna, left fragment of pe lvis, fragment of right tibia, frag zon and locality: Santa Cruz FOlmation, without. locality ment of left tibia, and right astragalu s. Horizon and locality: data (see Marshall. 1982). Santa Cruz Province. Santa Cruz Formation, Estancia La Costa Member, Fossil MicroNotherium gallegosense Sin clair. 1906 iferous Leve l 5.3, Puesto Estancia La Costa, Santa Cmz AMNH 9591, a right mandibular ramu s with p3- m2. Hori Province. zo n and locality: Santa Cruz F0l111arion, Estancia Felton, Santa Cruz Province. Dromiriops gliroides Thomas, 1894 REFERE N CES AbeJ!o, M. A. (20C)?). Sistematica y bioeslrmigrafia de los MACN 19142, MACN 2291 8. MACN 22919, a nd MACN Pallc ilubercul ata (Mamm.llia, M 169 170 Ma.rLa Alejandro. Abello el al. correcciones. Revisra Argemina de His(oria Natural, to Early- Middle Miocene (Deseadan-San!acrucian) 1,289-328 . Caenolestoid Marsupials of South America. Amico, G. C .. Rodriguez~C abal, M. A. and Aizen, M. A. (2009). Journal oj Po/aeol/rolog)' Memoir 29, 67, 1-76. The pOlenrial key seed·dispersing role of the arboreal Bozinovic. F., Ruiz, G. and Rosentnann, M. (2004). Energerics marsupial Dl'omiciops gliroides. Acta Oemlogica. and torpor of a SOLl th American " li ving fossil", the 35, 8- 13. microbiolheriid Dromiciops gliroides. Journal oj Amrine-Madsen, H. , Scall y, M., Westerman, M. et al. (2003). Comparafive Physiology B, 174, 293-297. Nuclear gene sequences provide evidence for the Charles-Dominique , P. (1983). Ecology and social monophyly of allstraiide iphian marsupials. Molecular adaptalion in didelphid marsupials: comparisons Phylogenclics alld Evolution, 28 , 186-196. with eUlherians of similar ecology. In Adl'Gl1ces in the Anderson, S. (1997). Mammals of Bolivia, taxonomy and Study of Mammalian Bellm'ior, ed. 1. F. Eisenberg. distribulion. Bulletin oj {he American Mlfseum of Na/ural ShippenSburg: Ame rican Society of Mammalogist, His/ory, 231, 1--652. pp. 305-422. A rgot, C. (2003a). PO .'Hcranial functional adaptarions in the South Charles·Oominique, P.. Atramenrowi cz, M. , Charles-Dominique, American Miocene borhyaenoids (Mammalia, Metatheria): M. el at. (1981). Les mammiferes frugi vo res arboricoles Cladosicfis, PseudoJloliclis and Sipalocyoll. Alcheringa, noctulT1es d' une forel guyanaise: inleH e larions pl antes 27 , 303- 356. anim.aux. Revue d' Ecologie (Terre Vie) 35, 341--436. Argot, C. (2003b). Funclional adaplalions of (he poslcrania l Churchfield, S. and Sheftel. B.1. ( 1994). Food niche overlap ske lelon of two Miocene borh yaenoids (Mammalia. and ecological se paration in a multi-species community Mela lheria), Borhyo('lfa and Profhyloeitlus, from 50mh of shrews in the Siberian laiga.1ournal ofZoology, America. Palaeontology. 46. 12 13-l267. 234. 105- 124. Asher, R.I., Horovitz, I. and Sanchel.·Viliagra. M.R. (2004). Churchtie ld , S .• Nesterenko V. A. and Shvarts, E. A. (1999). First combined cladistic analysis of marsupi al mammal Food niche overlap and ecological separalion amongst int erre l at i o n ~h ip s. Molecular Phylogenetics ol1d Evolution, six species of coexistin g forest shrews (lnsecllvora : 33, 240-250. Soricidae) in the Russian Far East. Jow'na! of Zoo[o/:y, August, P. v. (1983). The role of habital complexilY and 248. 349- 359. heterogeneity in struclUring tropical mammal communities. Croft. D. B. and Eisenberg, J. F. (2006). Behaviour. In Marsupials, Ecology. 64 (6), 1495- 1507 . ed. P. J Armall, C. R, Di ckman and I. D Hume. Cambridge, Bakker, V. J. and Kelt, D. A. (2000). Scale-dependenr pattems in UK: Cambridge UniversiTY Press, pp. 229- 298, body size distribut ions of Neorropical mammals. Ecology. Delciellos, A. C. and Vieira. M. V. (2006). Arboreal walking 81 ,3530-3547. performance in seven didelphid marsupials as an aspect Barkley, L. J. and Whitaker, 1. O. Jr. (1 984). Confinnmion of of their fundamental niche. AlJsfral Ec%g}', 31 , 449--457. Caellolestes in Peru with in formation on diet. Journal oj DeicielJos, A. C. and Vieira, M. V. (2009). Jumping ability Mamrrwlogy, 65, 328-330. in the arboreal locomotion of didelphid marsupials. Barreda, V. D. (2002). Palinofloras cenozoicas. In Geologia )' MasfOzoologlo Neorropical. 16, 299- 307. Recttl'sos Naf/Jr(lles de Sallfa Cruz, Refato,.io del XV Dickman. C. R. and Vieira, E. (2006). Ecology and life histories. COllgreso Geologico Argentlnu. ed. M.J. Haller. Buenos In Mal'.wpia/s, ed. 1. P. Armali. C. R. Dickman and L D. Aires: Asociaci6n Geol6gica Argentina, pp. 545- 567. Hume. Cambridge: Cambridge University Press, Barreda, V. and Palazl.esi, L. (2007). Patagonian vegetation pp. 199-228. turnovers during the Paleogene-earJ y Neogene: origin of Dimpel, H. and Calaby , J. H. (1972). FUllher observaTions on the arid-adapted flo ras. The Botanical Relliew, 73, 31 - 50. moum.ain pygmy·po:>sum (Bwrtlmys parvus). Victorian Beck, R. M. D. (2008). A dated phylogeny of marsupials using Naturofisl,89. 10 1- 106. Gain , F.1. (1997). New dues for understanding Neogene A. C. Wa lker. Pittsb urgh: Uni versity or Pittsburgh Press. marsupial rad iations. In A Hi.~tory of Ihe NeotropicaJ pp. 501-530. Fauna. Vertebrate Paleobiology of the Miocene in Kay, R. F. and Hylander, W. L (1978 ). The dental strncture of Colombia. ed. R. F. Kay, R. H. Madden, R. L. Cifell i and mammalian folivores wilh special reference to primates and 1. J. Flynn. Washi ngton: Smithsonian In:;;lilu[ion Press, Phaiangeroidea (Marsupialia). ln The Ecology oj Arboreal pp. 185-204. Folil'ores, ed. G. G. Montgomery. Washington D. C.: Gain, F. J. (2003). Early mars upial radiations in South .I\...lllerica. Smithsonian InSlitution Press. pp. 173-191. In Predators with Pouches: The Biology of Camil'orous Kay, R. F. . Madden, R. H., Van Schaik, C. and Higdon, D. (1997) , Marsupials, ed. M. Jones, C. Dickman and M .. Acher. Primate species richness is determined by plant Hobart, Anstralia: CS IRO Pnblishing, pp. 30-42. producti vity: Implications for conservation. Proceedings of Ga in, F. J., Candela, A. M ., Abello, A. and Oliveira, E. O. (2009). the Natiollal Academy o.fSciellce.\· . USA, 94, 13023-13027. Earliest Sourh American Paucitubercul atans and their Ke lt , D. A., Meserve , P. L. and Lang. B. K. (1994). Quantitative significance in the understanding of "pseudodiprotodont " habirat associations of small mammals in a remperate marsupial radiat.ions. Zoological JOl/mal of the LilUleon rainforest in .~ofl[h e m Chile: empIrical pallerns and the Society, 155. 867-884. importance of ecological scale. Journal of Mamma/ogy, Gain . F.J., Abello, M. A. and Chomogubsky, L. (20 10). 75, 890- 904. Middle Terriary marsnpials fro m centra l Patagonia (early Kirsch, J. A. W. and Waller, P. F. ( l979). Notes on the trapping and Oligocene of Gran Barranca): unde rstanding South behavior of the Caenoieslidae (Marsupialia). Journal of America's grande cOllpure. ln The Paleontology a/Gran Mammalo:?y, 60, 390-395. Barranca: Evolurion and Ellvironmenra l Change throllgh Lee, A. K. and Cockbllm, A. (1985). Evolutionary Ecology of tlte Middle Cenozoic of Patagonia, ed. R. H. Madden, Marsupials. Cambridge: Cambridge Uni versiry Press, A. A. Carlini, M. G. Vucerich and R. F. Kay. Cambridge: Mann, G. (1955). Monito de l monte Dromiciops australis Philippi. Cambridge Uni versity Press. pp. 69-1 05. In wwigaciones ZooloRicas Chi/enas, 2, 159- 166. Goin, F. J., Zirnicz, A. N., Forasiepi , A. M., Chomogubsky, L Marshall, L. G. ( 1976a). Revi!'ion of the South American Fossil and Abello, M. A. (in press). The rise and fall of South Marsupial sub famil y Atxlerili nae (Mammali a, American Metatherians: contex(s, adaptations. rad i ation~, Ctlenolestidae). Publicat:ioll.e s del Museo Municipal and extinctions. In Origins and Evollllian ofCenozoic SO l/th Ciencias Nawmles "Lorenzo Scaglia," 2, 57-90. American Mammals. ed. A. L Rosenberger and M. F. Marshall, L. G. ( 1976b). Fossil localities for Santacrucian Tejedor. Verrebrale Paleohiology and Paleoanthropology (early Miocene) mammals, Santa Cruz Province, southem series. Dordrecht: Springer. Patagonia, Argentina. Journal of Pa!eol1lolo/:y, 50, Grand. T. I. ( 1983). Body weight: irs relationship [ 0 tissue 1129-11 42. composition, segmental distribution of mass and motor' Marshal!, L. G. (1980). Systematics of the South American func tion. II1. The Didelphidae of French Guyana. marsupial fa mily Caenolestidae. Fie/diana Geology Australian Journal a/Zoology. 3l, 299- 312. (new series), 5, 1- 145. Greer, .J. K. (1966). Mammals of Malleco Province, Chile. Marshall , L.G. (1982). Systematics ofrhe South American Publications of the Museum of Ihe MichiRan State marsupial family Mi crobiotheriidae. Fieldialla Ce%RY, Unil'ersity (B iological Series), 3, 49- 152. 10, 1-75. Heesy, C. P. (2008). Ecomorphology of orbit oricOlation and rJl e Meredith , R. W., Weste lman, M" Case, J. A. and Springer, M. S. adaptive significance of bjuocular vision in primates and (2008). A phylogeny and ti mescale for marsupial evolntiou other mammals. Brain, Behavio/' and Evolurion, 7l, 54-67. based on sequences for fiv e nuclear genes. JOllrnal 0/ Hershkovitz, P. (1999). Dramiciops gliroides Thomas, 1894, last of Mammalian Evolution, 15, 1- 26. t..he Microbiotheria (Ma rsupialia), with a review of the family Meserve, P. L., Lang, B. K. and Patterson, B. D. ( 1988). Trophic Microbiotheriidae. Fieldiana Zoology (new series), 93 , 1--60. rela tion ship~ of small mammals in Cl Ch ilean temperate rain Horovirz, I. and Sanchez-Villagm, M.R. (2003). A morphologicnl fo re:;; t. Journal of Mamma logy, 69, 721-730. analysis of marsupial mammal higher-level phylogenetic Miles, M.A.. Sousa, A. A. and P6voa, M. M. ( 198 1). Mammal relationsh ips. Cladistics, 19, 18 1-2 12. tracking and nest location in Brazilian fore st with an improved Hume, I. D. (2003). Nutrition of carni vorous marsupial s. In spool-and-line device. JOllrnal of Zoology, 195, 33 1- 347. Predators with pouches: (he biology of carnivorous Miranda, C. L., Rossi, R. V., Silva Junior, J. So., Lima, M. G. M. marsllpia!s, ed. M. Jones, C. Dickm an and M. Acher. and Santos. M. P. D. (2009). Mammalia. Didelphimorphia, Hobart.. Australia: CSIRO Publishing, pp. 22 1-228. Didelphidae, Metoch irus 11IldicrJ/Jdalus, Municipalit y of Hume, I. D. (2006). Nutrition and dige~tion . In Marsllpials. ed. Jose de Freitas, State of Piau!, Northeastern Brazil: J. P. Arn1ari , C. R. Dickman and r. D. Hume, Cambridge: Distribution extension. Check LiJ/, 5, 360- 363. Cambridge University Press, pp. 137-158. Moraes, E. A. Jr. (2004). Radio tracking of one MelOchirtlJ Kay, R. F. and Hiiemae, K. (1974). Mastication in Galogo nudic(Juda(Us (Desmaresl. 1817) individual in Atlantic crassicaudalUs: a cinefl ourographic and occlusal study. Foresl of Southeastern Brasil. Boletim do Museu de In Prosimian biology, ed. R. D. Man il1 , G. A. Doyle, and Biologia Mello Leila-o, 17 ,57- 64. 172 Modo Alejandro Ahello et a1. Nilsson, M. , Amason. U., Spencer, P. B. S. and Janke . A. (2004). RodrIguez-Cabal, M. A., Amico , G. C, Novara, A. J. and Aizen, Marsupial re lati onships and a time line for marsupiaJ M. A. (2008). Population characl.enslics of Dromiciops radial ion in Soulh Gondwana. Gene, 340, 189- 196. gliroides (Philippi. 1891), an endemic In arsupial of the Nilsson. M. A. , Churako\', G .. Sommer, M. el al. (2010). Tracking temperate fore st of Patagonia. Mammalian Biology, Marsupial evolulion us ing archaic genomic relroposon 73, 74-76. insertions. Plos Biolo/O', S. e I000436. Sanson, G. D. ( 1985). Functional de ntal mo rphology t1.nd diet Orti z-laureguizar, E. (2003). Relacioues de simiJitud, seleclion in dasyurids (Marsupia lia: Dasyuridae). paleoecologia y eX lincion de los Abderitidae (Marsnpialia. Auslralian Mammalogy, 8, 239- 247. Pauciruberc ul ata, Caenolesloidea). Co{oqIlios de Simpson, G. G. (1933). The " Plagiaulacoid" type of mammalian Po/eontolog/a (Vol. EXlC), 1, 475--498. dentition. Journal of Mamm.alogy. 14, 97- 107. Oniz-Jaureguizar, E. and Cladera. G. (2006). Paleoenvironmental Sinclair, W.J. (1906). Marsupialia of the Salll tl. C ruz beds. In evolution of sQ uthem South America during Ihe Cenozoic. Repol"fs oftbe Princeton University £rpeditions of iotrrl1C1I of Arid EnviroNments, 66, 489-532. Patagollia /896-1899. Vol. 4. Palaeonlology I. Part 3. Paiazzesi, L. and Barreda, V. (2007). Major vegelarion trends ed . W. B. Scot!. Princelon: Plinceton Universit y Press, in [he Tertiary of Patagonia (Argentina): il qlHllitati ve pp. 33~60. paleoclimatic approach based on palynological evidence. Smilh, A. P. and Lee, A. ( J984). The evolution o f strafegies Flora. 202, 328- 337. for survival and re production in possums and gliders. Parker, S. A. (1973). An annotated checklist o f the mammals o f In POSS UIl1.~ and Glidas, ed. A. Smilh nnd r. Hume. tile Northern Te rri to ry. Records of the Soufh Auslralia/1 Chipping No rLon, A uslral ia: Surrey Beatty and Sons, Museum , 16, I- 57. pp. 17- 34. Pascual, R. and Bond, M. (J 986). Evolucion de los mar:;upiales Staver. C A., Bond. W. J. , SLack, W. D ., van Rensbnrg, S. J. cenolOicos de Argentina. IV Congrcso Argentino d~ and Waldram, M. s. (2009). Browsing and tire interact to Paleonrolof? I{1 y Bioesr,.aligmf/(I, Mendoza, Ac(a'> 2. suppress tree dens ity in an African savanna. Ecological 14}-150. Applications, 19 0), 1909-J91 9. Pascual, R. and Ortiz-Jaureguizar, E. (1990). Evolving c1im,"Il es Strait, S.G. ( 1993a). Diffe rences in occlusal morphology and Rnd mammal fa unas in Cenozoic South America. Jouma/ molar size in frugivores and Faunivores . .fOWl/al 0/H llman of Human Em/utio/!, 19, 23--60. Evo/ution, 25, 471-484. Pascual, R., Oniz-Jaureguizar, E. and Prado. J. L. (1996). Slrai!. S.G. (1993b). Molar morp hology and food lexture among Land m<-lmmals: Paradigm of Cenozoic South American small bodied inseet ivorous mammals. ./OUI"IIO/ of geobiotic evolution. In COII(l"ihu tion of Soufltem South Mammalogy, 74 , 39 1-402. America fO Ve,.tebrate Paleontology, ed. G . ArratiR . Szalay. F. s. (1982). A new appraisal o f marsupial phylogeny and Munchen: Muncher GeowissenscafLljche Abhandlnngen classificalion. In Cctnlll'orolJs Marsupials, ed. M. Archer. (A) Verlag D r. Fiedrich Pfeil, 30. pp. 265-319. Sydney, Auslralia: Royal Zoological Society of New South Patterson, B. D. (2007). Order Paucituberculata Ameghino, Wales, pp. 621-O4{). 1894. fn Mammals of SOlllh America, Vol. l. Marsllpials. Szalay, F. S. (1994). El'O/lIlioIlO1Y History ofthe Marsupials and Xeflorrhralls, Shrews. and Bars, ed. A. L. Gardner. Chicago an AI1t1IYJis o/Osteological Characters. New York: and London: Uni versil), of Chicago Press, PI>. 119- 127. Cambridge University Press. Pauerson, B. D. and Gallardo, M. H. (1987). Rhyncholes(es Szalay, F. S. and Sargis. E. J. (2001). Model-based analysis of raphal1lll"lls. Mmllmalian Species, 286, 1-5. postcra nial osteology of marsupials from the Paleoce ne Pallers.on, B. D. and Rogers., M. A. (2007). Order Mi crobiOl he ria o f ha boral (Brazil) and the phylogenetics and biogeograpby Ameghino. 1889. In M(lJ1Yl1als of SOUl II America. Vol. I . o f Me[atheria. Geodil'ersitas, 23, 139-302. Marsupials, Xellarihralls, Shrews, Gil d BOiS, ed. A. L. Tauber. A. A. ( 1997). PaleoecologIa de la Formac ion Santa Cruz Gardner. Chicago and London: University o f C hi cago (Mioccno luferior) en el extremo sudesre de la Patagonia. Press, pp. 11 7-119. Ameghillialla, 34, 517-529. Perez, M. A. (20 10). Sistematica, ecologra y bioestratigrafia de Vieira, E. M. and Astua de Moraes. D. (2003). Camivory and Eocardiidae (Rodentia. Hystricognathi, Cm-ioidea) del insectivory ill NeotropicaJ marsnpials. In Predators with Mioceno feIT/pro.fl o ). media de Patagonia. Unpublished pouches: the hiology of carnivorous marsupials, ed. DocloraJ thesis. UnJ vers id<-ld Nacional de La Plaia. M. Jones, C Dickman and M. Acher. Hobart, Australia: Phi llips, M. J., McLenachan. P. A. , Down. c.. Gibb, G. C and CSIRO hblishing, pp. 267- 280. Penny, D. (2006). Combined mirochoudrial and nuclear Vieira, E. M. and Monteira-Filho. E. L. A. (2003). Vertical DNA sequences resolve the interrelations of the major malificalion of small mammals in the Atlantic rain forest Australasian mar5upial radiations. Sysremalic BloloRY. o f so uLh-easte rn Brazil. Journal of Tropical Ecology. 19, 55. 122- 137. 501- 507. Ramirez, 0 ., Arana. M., Bazan . E. , Ramirez., A. and Cano, A. We bb, S. D. (1978). A history of savanna vel1 e brales in the (2007). Assemblages of birds and mammals communities New W orld. Pari II: South America and the GreaL ill two major ecological unirs of the Andean highland lnten.:hange. Atmual Review (if Ecology and Syslemarics. 9, plateau of southern Peru. EcolaglQ Aplicada, 6, 139-148. 393-426.