AMERICAN MUSEUM Novitates

PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024

Number 3460, 17 pp., 4 figures, 4 tables October 28, 2004

Comparative Postnatal Ontogeny of the Skull in Dromiciops gliroides (Marsupialia: Microbiotheriidae)

NORBERTO P. GIANNINI,’ FERNANDO ABDALA,? AND DAVID A. FLORES?

ABSTRACT

Dromiciops gliroides is the single extant representative of the marsupial family Microbioth- erlidae. The importance of D. gliroides stems from its peculiar cranial anatomy (specifically the configuration of the tympanic region) and dentition and from its controversial position in the phylogenetic tree of marsupials—a South American form more closely related to Austra- lasian marsupials. We studied the postnatal ontogeny of the skull in D. gliroides by analyzing qualitative and allometric aspects of the development of cranial structures. We compared re- cently weaned young individuals with adults and described the bivariate and multivariate allometric trends of 14 cranial dimensions for a sample of 37—51 specimens. Most cranial components develop in a way similar to didelphids studied so far. However, some trends (e.g., growth of the orbit) seem particular to D. gliroides. The microbiotheriid bulla of D. gliroides, a structure to which five basicranial bones contribute parts, is already present in its highly derived condition in the youngest specimens of our series. We conclude that except for the bulla, most of the cranial development in D. gliroides is highly conservative and that some peculiarities may be shared with other marsupials of similarly small body size. Data on aus- tralidelphians and small-size didelphids are needed to contrast these patterns.

' Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History; Programa de Investigacion de Biodiversidad en Argentina, Facultad de Ciencias Naturales, Universidad Nacional de Tucuman, Miguel Lillo 205, Cédigo Postal 4000, Tucuman, Argentina (norberto@amnh.org).

? Bernard Price Institute for Palaeontological Research, University of the Witwatersrand, Private Bag 3, WITS 2050, Johannesburg, South Africa; Programa de Investigacién de Biodiversidad en Argentina, Facultad de Ciencias Naturales, Universidad Nacional de Tucuman, Miguel Lillo 205, Cédigo Postal 4000, Tucuman, Argentina (abdalaf@ geosciences. witz.ac.za).

3 Division of Vertebrate Zoology (Mammalogy), American Museum of Natural History; Programa de Investigaci6n de Biodiversidad en Argentina, Facultad de Ciencias Naturales, Universidad Nacional de Tucuman, Miguel Lillo 205, Cédigo Postal 4000, Tucuman, Argentina (dflores@amnh.org).

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INTRODUCTION

The marsupial Dromiciops gliroides, a small South American endemic, is the single survivor of the Microbiotheriidae, cohort Mi- crobiotheriomorpha Ameghino, 1887. The other 5 (Marshall, 1982) to 13 (Hershkovitz, 1999) forms of microbiotheres are fossils from the Tertiary of Patagonia, Argentina (Marshall, 1982), and Seymour Island, Ant- arctica (Goin et al., 1999). Dromiciops gli- roides occurs in Chiloé Island, continental Southern Chile, and adjacent parts of Argen- tina (Marshall, 1978). Reig (1955) first rec- ognized the affinities of D. gliroides with mi- crobiotheres, primarily on the basis of the structure of the tympanic bullae and molar shape. Microbiotheres were considered by Reig et al. (1987) and Hershkovitz (1992, 1999), among others, to be closely related to didelphoids—members of the family Didel- phidae and allies. By contrast, Szalay (1982), who examined ankle-joint morphology, pro- posed the inclusion of D. gliroides in the co- hort Australidelphia—a monophyletic group including all Australasian marsupials. In most recent studies, D. gliroides consistently appears more closely related to australidel- phians than to didelphoids (e.g., Rougier et al., 1998; cf. Colgan, 1999). However, there is disagreement with regard to the exact placement of this form. D. gliroides is either the sister taxon of all australidelphians (Re- tief et al., 1995 [part]; Palma and Spotorno, 1999 [part]; Amrine-Madsen et al., 2003), or it is nested within australidelphians, usually as sister to Diprotodontia (Kirsch et al., 1991; Retief et al., 1995 [part]; Palma and Spotorno, 1999 [part]; Jansa and Voss, 2000; Horovitz and Sanchez-Villagra, 2003).

Most studies on Dromiciops gliroides have emphasized the anatomical differences of this form with other South American mar- supials. In a detailed study of the middle ear, Segall (1969) found support for Reig’s (1955) contention that the bulla of D. gliro- ides is microbiotheriid-like. Marshall (1982), in his systematic revision of microbiotheres, included a diagnosis of D. gliroides with a brief account of anatomical features of the skull and dentition, and he reported morpho- logical differences between D. gliroides and Microbiotherum. Hershkovitz (1992, 1999)

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carried out two anatomical revisions discuss- ing the phylogenetic position of D. gliroides (although not on the basis of a numerical character analysis), reporting putative auta- pomorphies and symplesiomorphies in oste- ology, dentition, soft anatomy, and serology.

In spite of this body of anatomical work, little is known about the ontogeny of D. gli- roides. However important in itself, the phy- logenetic and biogeographic relevance of D. gliroides makes the understanding of devel- opment in this species particularly signifi- cant. In this work, we report postnatal onto- genetic data on skull morphology, a part that provides some of the most distinctive ana- tomical features of D. gliroides (Reig, 1955; Segall, 1969; Marshall, 1982; Hershkovitz, 1999). To our knowledge, this also represents the first study of an australidelphian for which data on skull ontogeny are approxi- mately comparable to those available on di- delphids (cf. Moeller, 1973). Qualitative and allometric analyses of growth allowed us to explore how distinctive the skull develop- ment of D. gliroides is in a context of com- parative ontogeny. On the basis of our pre- vious work on large-sized didelphids (Abdala et al., 2001; Flores et al., 2003), we show that the overall pattern of skull growth in D. gliroides is highly conservative. In turn, we contend that a minority of the observed de- velopmental trends may be uniquely derived, but this remains to be contrasted with yet un- known ontogenetic patterns of small-sized didelphids and australidelphians.

MATERIALS AND METHODS STUDY SPECIMENS

We analyzed a sample of 51 specimens of Dromiciops gliroides from Chile and Argen- tina housed at the following U.S. and Argen- tinian collections: American Museum of Nat- ural History, New York (AMNH); Centro Regional Universitario Bariloche, Bariloche (CRUB); Colecci6én Mamiferos Lillo, Tucu- man (CML); Field Museum of Natural His- tory, Chicago (FMNH); Instituto Argentino de Investigaciones en Zonas Aridas, Men- doza (IADIZA); Museo Argentino de Cien- cias Naturales Bernardino Rivadavia, Buenos Aires (MACN); and National Museum of Natural History, Smithsonian Institution,

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Washington, D.C. (USNM). The specimens

examined were AMNH 92147; CML 1869, 6217-8; CRUB 11, 12; FMNH 22671, 22673, 22675, 50073—5, 127436-8, 127440, 127443-8, 127450, 127451, 127453-5, 127457-—65, 129803, 129804, 129806-8, 134556, 48.26, 13308, 19142-5; and USNM 391772.

Seventeen specimens in our sample do not

have a fully adult dentition, whereas the re-

maining individuals were adults of varying sizes. The young specimens were in an age stage in which, according to Mann-Fischer (1978) and Mufioz-Pedreros and Palma

(2000), they could move outside the mother’s pouch. The smallest individual (CML 6217; total length of skull 20.1 mm) has I5 and M2 in the process of eruption, with the latter hav- ing the protocone not yet totally emerged. The difference in size between CML 6217 and the largest specimen (AMNH 91147; to- tal length of skull 29.8 mm) implies that the smallest specimen had achieved only approx- imately two-thirds of its maximum adult size,

suggesting that the size range of our sample

is appropriate for an analysis of postweaning growth.

QUALITATIVE DESCRIPTIONS AND ALLOMETRY

In this study, we took two descriptive ap- proaches. First, we contrasted developing features in the skull of smallest (youngest) specimens with those of the largest (oldest) on a qualitative basis. Anatomical terminol- ogy follows primarily Wible (2003) and also Sanchez-Villagra and Wible (2002). Second, we used a series of quantitative linear mea- surements (fig. 1) to estimate allometric growth of skull components. We took two approaches to study allometry: bivarite and multivariate. For the bivariate treatment, we

used total length of the skull as a measure of overall size (Abdala et al., 2001; Emerson

and Bramble, 1993). In order to estimate the

change of each of the other cranial variable

with respect to overall size, we used the log transformation of the power growth equation y = boxe, where y is the focus variable, b, is the y-intercept, x is the total length of the

skull, b, is the slope of the line or coefficient

of allometry, and e is the error term. We as- sessed deviations from isometry by testing

134624; IADIZA 2526; MACN

GIANNINI ET AL.: DROMICIOPS GLIROIDES é

abe i |. (j y O é AP Cay » f) 3S? —~ 7 os a BP\—- \ :

aS BBu

Vay

4 ie: “t MA Ny u(/v Sy eth a UU MAAR

Fig. 1. Cranial measurements of Dromiciops gliroides used in this study. Abbreviations: BB, breadth of braincase; BBu, breadth of bulla; BP breadth of palate; BZ, maximum breadth of the skull, or zygomatic breadth; HC, height of coro- noid process; HD, height of mandible; HM, height of muzzle; HO, height of occipital plate; LB, length of bulla; LD, length of mandible; LN, length of nasals; LO, length of orbit; LP, length of lower postcanine row; PAL, length of palate; TL, total length of the skull; UP, length of upper postcanine row.

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the significance of the allometry coefficients (two-tailed f-tests) under the null hypothesis b, = 1.0 fixing type I error rate at a = 0.01 (for decreasing the chance of multiple com- parisons errors). Additionally, we considered marginally significant those coefficients that yielded 0.05 > P > 0.01. Isometry is the condition in which an allometry coefficient is statistically indistinct from unity. Statisti- cally significant deviations from unity rep- resent cases of “negative” allometry if b, < 1.0 and “positive” allometry if b, > 1.0. Following Abdala et al. (2001), we used two ways to calculate b,. Under the first ap- proach—least-squares regression (hereafter LS)—an independent variable x, chosen to represent overall size, is assumed to be mea- sured without error, therefore transferring the full error component to the response variable y. Under the second approach—reduced ma- jor axis regression (hereafter ,RMA)—the two variables involved in a bivariate rela- tionship, now y, and y,, are interchangeable. That is, the dependence relationship on size is not explicit; residuals are oblique compo- nents representing variation in both y, and y,. LS and RMA coefficients are arithmetically related through the correlation coefficient r (Niklas, 1994). Due to this relationship, dif- ferences between LS and RMA are mere scale shifts along the variation of b, whose magnitude depends on the amount of varia- tion explained by size (i.e., on the size of the r value). As a consequence, we interpret bi- variate allometry depending on the strength of the relationship found in both methods. Our multivariate approach to allometry is based on the generalization of the allometry equation proposed by Jolicoeur (1963a, 1963b; see applications in Voss et al., 1990; Voss and Marcus, 1992). In bivariate allom- etry, one variable is set apart representing size, and allometry of all other variables is estimated one by one with respect to that chosen variable. By contrast, in multivariate allometry, size is regarded as a latent vari- able affecting all original variables simulta- neously. The various allometric relationships of all variables with the latent size can be expressed in the first eigenvector of a prin- cipal components analysis, with this vector extracted from a variance-covariance matrix of log-transformed variables and scaled to

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unity (i.e., with all elements scaled so that the sum of squared elements equals 1; Joli- coeur, 1963a). Allometry is, in this approach, a deviation with respect to a hypothetical iso- metric eigenvector that represents pure size change. Under isometry, all variables re- spond the same way to growth; the elements of the isometric unit eigenvector are equal to an expected value calculated as 1/p®°° with p equal to the number of variables. The value of an element of the sample eigenvector rep- resents the observed multivariate coefficient of allometry of the corresponding variable. We were specifically interested in the devi- ations from multivariate isometry of each of the skull variables used in our bivariate anal- yses (bullar dimensions excluded). For that purpose, the first unit eigenvector was ex- tracted from a variance-covariance matrix calculated on values of the 14 variables (in- cluding total length of the skull) transformed to the natural logarithms. Because principal components analysis requires a complete de- sign (i.e., no missing data), we performed our analysis with the subset of 37 specimens having measurements for all 14 skull vari- ables.

The elements of the hypothetical isometric vector are equal to 0.267 since p = 14. Com- parison of each of the empirical elements of the first-unit eigenvector with the isometric eigenvector allows to detect negative (<0.267) and positive (>0.267) departures from isometry in each original variable. However, multivariate coefficients of allom- etry are single values that come from a one- sample estimation. As such, deviations from isometry can only be assumed. The number of D. gliroides specimens is too limited to draw adequate subsamples and calculate standard confidence intervals for multivariate coefficients, which would allow for an isom- etry test. Instead, we adopted a resampling strategy based on the jackknife (Tukey, 1958). This technique transforms any prob- lem of estimation into the estimation of a sample mean (Manly, 1997). As applied to our study, a set of pseudovalues (surrogates of the true coefficients of interest) are cal- culated by successively removing one spec- imen at a time from the sample (first-order jackknife) and calculating the subsample unit eigenvector as established above. Specifical-

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ly, one pseudovalue €*,, corresponding to the removal of specimen j from the sample of size n, is calculated as

AK As Bs fuel) Aw 5. ae =. = sles,

where é is the observed element of the unit eigenvector that corresponds to the multivar- iate coefficient of allometry of the skull var- iable x, and €_,; is the value of the coefficient obtained with specimen j removed (termi- nology follows Manly, 1997). Then, the set of 1 to n pseudovalues (n = 37, the number of specimens in our sample) is used for two purposes. First, for a given variable, the mean of the corresponding pseudovalues rep- resents the jackknife estimate of the multi- variate allometry coefficient of that variable, and the difference between that mean and the observed coefficient of allometry is an esti- mate of the sampling bias that may be pre- sent in the one-sample coefficient derived from the analysis including all specimens (Quenouille, 1956; Manly, 1997). Second, the set of pseudovalues can be used to cal- culate a standard deviation, and then a con- fidence interval, for each coefficient of al- lometry. We considered as a departure from isometry the case when the 99% confidence interval for a coefficient did not include the expected value under isometry (0.267). Further considerations are necessary. When standard deviations are calculated by resampling, confidence intervals may be se- verely influenced by extreme values (Manly, 1997). This is particularly true when the total number of resampled values is not large, as in the first-order jackknife. Trimming the m largest and the m smallest values tends to ameliorate this problem (Manly, 1997: 44). The justification of this practice lies in the observation that, as in any sampling prob- lem, if the m pseudovalues are not especially large or small in magnitude, trimming has a negligible effect on standard deviations and hence on the breadth of confidence intervals. But if the extreme pseudovalues are indeed unduly influential, trimming the m pseudov- alues effectively prevents large standard de- viations and exceedingly wide confidence in- tervals. Manly (1997) reported that taking out of the pseudosample even the minimal number of extreme pseudovalues yielded sat- isfactory results. We report 99% confidence

GIANNINI ET AL.: DROMICIOPS GLIROIDES 5

intervals for each multivariate coefficient of allometry based on all pseudovalues (un- trimmed set) and in a set taking m = 1 pseu- dovalues out (trimmed set; table 2). In all analyses, we assume that there are no growth-independent shape differences among sexes and localities. In support of these as- sumptions are the facts that D. gliroides lacks sexual dimorphism (Hershkovitz, 1999) and that all but one specimen in our sample (FMNH 127465, from Chiloé) were collected in continental localities. That specimen may be influential only in the breadth of palate (see fig. 4A). For our analysis of multivariate allometry, we used the program NTSYS-pc 1.6 (Rohlf, 1990). The jackknife procedure was done partly manually and partly with the help of a NTSYS batch file.

Finally, we compared both our quantita- tive and qualitative results in D. gliroides with the developmental trends known from two didelphid marsupials, Didelphis albiven- tris (Abdala et al., 2001) and Lutreolina crassicaudata (Flores et al., 2003). Unfortu- nately, there are no published studies dealing with skull allometry in australidelphian mar- supials in a similar way, so our comparisons must be restricted to didelphids. To our knowledge, only a single study of cranial al- lometry in australidelphians exists, specifi- cally on dasyuromorphans (Moeller, 1973). However, in that study, the independent var- iable selected for the bivariate estimation of skull allometry was atypical—the length of the brain cavity—thus complicating compar- isons with our results.

RESULTS AND DISCUSSION QUALITATIVE TRENDS

OSSIFICATION: In the youngest specimen (CML 6217), part of the zygomatic arch, the lateral side of the braincase, the mastoid por- tion of the petrosal, the lacrimal, part of the alisphenoid, and the orbitosphenoid are poor- ly ossified. Most of these are neurocranial components, so our observations are in agreement with the model of delayed growth (both in timing of onset and in rate of ossi- fication) proposed for marsupial neurocranial development by Clark and Smith (1993).

TEETH: Most of the teeth in our juvenile sample are contiguous. Only a small diaste-

6 AMERICAN MUSEUM NOVITATES

ma appears between the last upper incisor (IS) and the canine (C). In adults, there are enlarged diastemata between I5 and C and among the upper and lower premolars (fig. 2). Therefore, the spacing among several teeth modestly increases with age in response to the continuing growth of the supporting bone.

SPLANCHNOCRANIUM: The mandible shows important modifications in the development of coronoid and angular processes (fig. 2, cf. D and H). In adults, the bone in the pars molaris of the mandible is thicker, the coro- noid process is higher, and the angular pro- cess is longer than in younger individuals, both in relative and absolute terms (see also Allometry below). The caudal margin of the mandibular symphysis in the young speci- mens is at the level of the canine (fig. 2D); in the adult, that margin is slightly displaced caudally to the level of pl (fig. 2H).

In young animals, the angular process of the mandible closely fits in the globular shape of the bulla. This mandible-otic con- nection was interpreted in functional terms by Maier (1987, 1990), who proposed that the pouch young might first hear sounds transmitted by the mandible. However, San- chez-Villagra and Smith (1997) rejected this hypothesis on the basis of measurements of the auditory capacity of developing young, but they did not provide an alternative hy- pothesis. In D. gliroides, the developing mandible soon detaches from the ear region, so that in adults the contact between the bulla and the angular process is lost, causing the isolation of the bulla from the mechanics of the mandible. According to Sanchez-Villagra and Smith (1997), this developmental pro- cess is common to all known marsupials.

In adults, an excavated mandibular notch notably separates the articular condyle from the coronoid process. The condyle of adults is more laterally expanded than in juveniles (fig. 2, cf. D and H). The postglenoid pro- cess, weak in juveniles, is enlarged in adults (fig. 2, cf. C and G). Abdala et al. (2001) and Flores et al. (2003) observed these changes in two didelphids and proposed that the ad- justment of the jaw articulation through the expansion of the condyle facilitates the safe- ty of the mandibular movements during strenuous bites. A functionally related

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change is the development of the masseteric line in adults, for insertion of the deep mas- seter muscle (based on Didelphis marsupi- alis; Turnbull, 1970).

NEUROCRANIUM: The foramen magnum is bordered by the basioccipital ventrally, the exoccipitals laterally, and the supraoccipital dorsally, in all observed growth stages (fig. 3). This condition is also present in all small- sized didelphids (Gracilinanus, Marmosa, Marmosops, Micoureus, Thylamys, Mono- delphis, and Lestodelphis; Flores, 2003). In contrast, in large-sized didelphids (e.g., Di- delphis, Lutreolina), there is an ontogenetic exclusion of the supraoccipital so that only exoccipitals contribute to the dorsal rim of the foramen magnum in adults (Abdala et al., 2001; Flores et al., 2003). Therefore, the con- dition in D. gliroides may be correlated with its small size. Alternatively, this may repre- sent a plesiomorphy, given that in adults of the Paleocene metatherian Pucadelphys an- dinus, also a small form and sister to Mar- supialia (Horovitz and Sanchez-Villagra, 2003; Rougier et al., 1998), the supraoccip- ital forms the dorsal margin of the foramen magnum (Marshall and De Muizon, 1995).

In adult D. gliroides, the sphenorbital fis- sure is virtually coalesced with the foramen rotundum; only a tiny bony wall deep inside the fissure, not apparent in lateral view, bare- ly separates the two openings. Unfortunately, the condition in the youngest specimens can- not be assessed due to poor preservation of the bone in the pterygopalatine fossa. By contrast, in most adult didelphids, these openings are close together, but the bony wall that separates them is noticeable in lat- eral view (personal obs.). All basicranial fo- ramina (the foramen ovale, carotid, jugular, and hypoglossal foramina, and the transverse canal) are already in place in the juvenile. Dromiciops gliroiodes lacks secondary fo- ramen ovale; there is only a sulcus for the exit of the mandibular ramus of trigeminal nerve (V°), located in the anterior part of the tympanic wing of alisphenoid. The sulcus is present in juveniles.

Dromiciops gliroides is unique among marsupials in having a sphenoid crest—a ventral, median ridge of the presphenoid and basisphenoid in the basipharyngeal duct (this structure, however, is widely distributed

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among eutherians; Hershkovitz, 1992). The sphenoid crest is already present in juveniles, although less marked in comparison with the adult condition.

AUDITORY BULLA: The bulla of D. gliro- ides is illustrated in Hershkovitz (1999: fig. 7A)* and in Sanchez-Villagra and Wible (2002: fig. 11). In adult D. gliroides, the bul- la is a ventrally closed, globular structure formed by four components: the ectotympan- ic (lateral), the tympanic process of the ali- sphenoid (anterior), the caudal tympanic pro- cess of the petrosal (posterolateral), and the rostral tympanic process of the petrosal (me- sial and ventral; Sanchez-Villagra and Wible, 2002). Additionally, two small processes, one from the basioccipital and another from the exoccipital, complete the sealing of the bulla at its contacts with the basicranium— sutures only interrupted by the jugular fora- men. The young specimen features two main differences with the adult in relation to the bulla. First, the opening of the external acoustic meatus in the young is delimited only by the ectotympanic. Toward adulthood, the tympanic process of the alisphenoid and the caudal process of the petrosal grow over the ectotympanic as the pneumatization of the bulla increases, so the opening of the ex- ternal acoustic meatus is smaller than in young individuals in absolute size. The ec- totympanic is then partially concealed in adults, its ventral portion being no longer visible externally. Second, the surfaces of the rostral and caudal tympanic processes of the

4In Hershkovitz’s illustration of the Dromiciops’ ba- sicranium, nomenclature of referred structures is either incorrect or inconsistent with Sanchez-Villagra and Wi- ble (2002), Wible (2003), or the Nomina Anatomica Ve- terinaria (1994; N.A.V.) in the following cases: refer- ence 14 is the sphenoid crest, not presphenoid (crista) or basisagittal crest of figure 8 in the same study (since the crest is also formed by the basisphenoid, the term crista sphenoidalis of the N.A.V. [1994] seems more ap- propriate); reference 19 is the caudal tympanic process of the petrosal, not tympanic process of periotic; refer- ence 22 is exoccipital, not supraoccipital or exoccipital; reference 24 is rostral tympanic process of petrosal, not entotympanic; reference f is suprameatal foramen, not postglenoid foramen; reference h is carotid foramen, not foramen ovale; reference k + m is jugular foramen, not jugular foramen (k) separate from hypoglossal foramen (m); reference | is hypoglossal foramen, not stylomas- toid foramen; reference n is foramen ovale, not carotid foramen.

GIANNINI ET AL.: DROMICIOPS GLIROIDES vi

petrosal are not distinct in the youngest spec- imens. This may suggest that both processes are actually a single unit that becomes sep- arated with age. In the adult, the suture co- incides with the location of the internal sep- tum of the bulla that overlies the bullar floor (likely homologous to the rostral tympanic process of the petrosal of other marsupials given its position rostral to the cochlear fe- nestra; see fig. 6 in Wible, 2003). An embry- ological study is necessary to fully under- stand the homology of the bullar floor.

The mastoid exposure of the petrosal, which covers the semicircular canals poste- riorly, is poorly ossified in the youngest spec- imen (CML 6217). All other specimens have already formed a thick wall of bone that is continuous with the caudal tympanic process of the petrosal (see fig. 3A, ref. a).

ALLOMETRY

BIVARIATE ALLOMETRY: The rate of change (allometric analysis) of each quantitative var- iable with respect to size (total length of the skull) is shown in table 1. The fit of the var- iables examined, as evaluated by the adjusted R? (coefficient of determination adjusted by df = N — 2), varied widely between 29 and 89% (fig. 4). In 8 out of 13 variables (not including the bullar dimensions), LS and RMA showed the same allometric trends. Specifically, both methods tended to reject isometry in the case of length of nasals (pos- itively allometric), breadth of palate, breadth of braincase, length of lower postcanine row, and height of occipital plate (negatively al- lometric; table 1). Both methods led to ac- ceptance of isometry in the length of palate, length of orbit, and breadth of zygomatic (ta- ble 1). The allometric trends in the remaining variables were as follows: the lengths of the upper postcanine row and mandible and the heights of the mandible and coronoid process were positive (or marginally so) under RMA and marginally positive or isometric under LS, whereas the height of muzzle was mar- ginally negatively allometric under LS and isometric under RMA (table 1).

MULTIVARIATE ALLOMETRY: Observed multivariate coefficients of allometry varied widely across variables (table 2). Two vari- ables, the total length of the skull and the

8 AMERICAN MUSEUM NOVITATES NO. 3460

ctop rtpp astp F

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breadth of zygoma, showed the smallest de- parture from isometry values. Average esti- mated bias (using absolute jackknife values) across coefficients calculated from trimmed and untrimmed values were both small and similar to each other (0.016 and 0.017, re- spectively). Conversely, trimmed pseudoval- ues did affect jackknife estimates of confi- dence intervals; the average standard devia- tion across coefficients from untrimmed pseudovalues was 3.2 times higher than from trimmed pseudovalues, and this difference is not attributable to outlying coefficients. The fact that only two skull variables can be char- acterized as allometric using an untrimmed set of pseudovalues is another suggestion that the breadth of confidence intervals may have been seriously affected. Extreme pseu- dovalues occurred mainly in pseudosamples in which the smallest specimen of the sample (CML 6217) was removed (46% of the 28 pseudovalues trimmed from the pseudoval- ues of the 14 variables used). This strongly suggests that, in order to obtain reasonable allometry estimates, the youngest specimen is indispensable, reinforcing the need for more specimens in that size range.

Considering then the (m = 1) trimmed analysis, which ignores all cases in which CML 6217 (and/or few other young speci- mens) were removed, several variables can be safely characterized as allometric (table 2). The breadth of palate, breadth of brain- case, length of lower postcanine toothrow, and height of the occipital plate were nega- tively allometric, whereas the length of the nasals and the height of the mandible were positively allometric. Notably, the set of al- lometric variables may also include the total skull length, but we must interpret this de- parture cautiously given that the upper limit of the 99% confidence interval for this var- iable almost includes the expected value un- der isometry.

<

GIANNINI ET AL.: DROMICIOPS GLIROIDES )

mep

astp rtpp

Fig. 3. Comparison of the occipital plate of young (A) and adult (B) Dromiciops gliroides. Abbreviations: a, schematic line indicating ap- proximate limit of mep and ctpp (see below); astp, tympanic process of the alisphenoid; bo, ba- sioccipital; ctpp, caudal tympanic process of pe- trosal; eo; exoccipital; ip, interparietal; mep, mas- toid exposure of the petrosal; pa, parietal; rtpp, rostral tympanic process of petrosal; sq, squa- mosal; za, zygomatic arch. Scale bars: 5 mm.

A comparison of bivariate and multivariate allometry (table 3) indicated that 8 out of 13 variables showed the same trend in multi- variate and both methods of bivariate allom-

Fig. 2. Comparison of skull shape in young (A—D) and adult (E—H) Dromiciops gliroides. Dorsal (A, E), ventral (B, F), lateral (C, G), and mandible (D, H). Abbreviations: an, angular process; astp, tympanic process of the alisphenoid; c, lower canine; Ca, upper canine; ctpp, caudal tympanic process of petrosal; dp3, lower deciduous third premolar; dP3, upper deciduous third premolar; M2, upper second molar; m3, lower third molar; p3, lower third premolar; P3, upper third premolar; rtpp, rostral

tympanic process of petrosal. Scale bars: 5 mm.

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10

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GIANNINI ET AL.: DROMICIOPS GLIROIDES 11

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NO. 3460

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2004

TABLE 3 Gross Comparison of Results Across Methods Used to Estimate Cranial Allometry in Dromiciops gliroides

Variables Multivariate RMA LS

Length of nasals + + (+) Height of muzzle = = (-) Length of palate = = = Breadth of palate - (-) s

Length of upper postcanine row = + =

Length of lower

postcanine row - - ~_ Length of mandible = (+) = Height of mandible + + = Height of coronoid

process = + = Breadth of zygoma = = = Breadth of braincase Heigth of occipital plate — _ ~ Length of orbit = a =

Symbols: =, isometry; +, positive allometry; (+), positive allometric trend (see text); -, negative allometry; (—), negative allometric trend (see text).

Abbreviations: RMA, coefficient of allometry under reduced major axis method; LS, coefficient of allometry under least squares method.

etry. The remaining variables were consistent with either RMA or LS estimates, and there was no case of a multivariate coefficient dif- ferent from both RMA and LS estimates. In 11 cases the multivariate trend is the same as in the least-squares regression, and in 10 cas- es the trend is the same as in reduced major axis regression (table 3). The small differ- ences between the multivariate and bivariate results are almost certainly due to the fact that, besides stochastic causes, bivariate al- lometry assumes isometry of the independent variable (total length of the skull), which is somewhat questionable in light of the trimmed jackknife analysis. Other variables, like the breadth of zygoma, may represent a more appropriate x-variable, if a bivariate analysis is desired.

We conclude that multivariate allometry is preferable, on grounds discussed in the meth- ods, over bivariate approaches. However, the latter are still useful principally because they are less affected by sample completeness, provided that the independent variable of choice is the closest possible to isometry. In

GIANNINI ET AL.: DROMICIOPS GLIROIDES 13

our analysis, a variable-wise sample size re- duction of 14—27% in the multivariate anal- ysis was caused by missing data in speci- mens. This is especially critical in fossils and in extant species in which specimens may be fragmentary as a consequence of their fra- gility. Also, examination of bivariate plots is highly useful.

QUANTITATIVE SKULL MODELING IN DRom- ICIOPS GLIROIDES: On the basis of the multi- variate analysis with trimmed jackknife es- timates of allometry, we describe the quan- titative trends in the modeling of the skull in D. gliroides as follows. The braincase is rel- atively smaller in adulthood, as indicated by the negative trend in breadth of the braincase and height of the occipital plate. By contrast, another neurocranial component—the or- bit—increases its length at a pace compara- ble to the increase in latent size, thus keeping the relative size of the eye socket constant. The palate becomes elongated in shape as a consequence of the isometry of its length and the strong negative allometry of its width. The upper toothrow is isometric, while the lower toothrow grows at a markedly slower rate than the latent size, likely because tooth emergence in the upper postcanine row is phased out with respect to the lower row— the lower row has one more tooth than the upper row, and so it shows a slower growth rate as to yield approximately the same ab- solute length in adults. In the other dimen- sions involving the muzzle, the nasals slight- ly increase their length whereas the height of the muzzle is isometric. Therefore, the entire muzzle grows isometrically except the palate, which decreases in width toward adulthood. The temporal space expands only a little giv- en that the braincase is negatively allometric while the zygomatic breadth is isometric. The mandible changes essentially by increas- ing its robustness, since the height of man- dible shows a positive trend, whereas the other two dimensions considered Cength of mandible and coronoid process) are isomet- rie.

On the basis of bivariate allometry, the bulla tends to grow with negative allometry along its length (b, varying from 0.61 to 0.86 depending on the regression method; table 1) and with a positive allometry along its width (b, varying from 1.06 to 1.35). In relative

14 AMERICAN MUSEUM NOVITATES

terms, the trend is toward a lateral enlarge- ment and longitudinal shortening of the bul- la, which is consistent with our qualitative observations.

COMPARATIVE ALLOMETRY: Bivariate allo- metric values from Abdala et al. (2001) for Didelphis albiventris (N = 61) and Flores et al. (2003) for Lutreolina crassicaudata (N = 43) allow us to attempt a comparison of al- lometric pattern with those didelphids. For- tunately, the youngest specimen of our sam- ple (CML 6217) exhibits a stage of tooth eruption roughly similar to the youngest specimens both in D. albiventris and L. cras- sicaudata. However, one aspect compromises the direct comparability of our results; al- though in Abdala et al. (2001), Flores et al. (2003), and the current work, total length of the skull was chosen as the estimator of over- all size, this measurement does not exactly correspond in the three studies and is there- fore not properly homologous. At any rate, dimensions spanning the entire length of the skull are known to be highly correlated, so an approximate comparison is still possible.

The coefficients for D. gliroides are con- cordant with either or both D. albiventris and L. crassicaudata in 11 of the 13 compared measurements (table 4). Of those 11 mea- surements, 6 show the same tendency in the three species. These are the isometric length of palate and zygomatic breadth; the nega- tively allometric breadth of palate and brain- case and the height of the occipital plate; and the positively allometric height of mandible. Dromiciops gliroides shares slightly more al- lometric trends with L. crassicaudata (9 var- iables overall, 3 variables exclusively) than with D. albiventris (8 variables overall, 2 variables exclusively; table 4).

Two variables define the most striking dif- ferences in coefficient values between D. gli- roides and both D. albiventris and L. cras- sicaudata. First, the development of the orbit is isometric in D. gliroides and strongly neg- atively allometric in the two didelphids (Ab- dala et al., 2001; Flores et al., 2003). This difference goes beyond this interspecific comparison, since the “negative” allometry of the orbit is a virtually general pattern in vertebrates (Emerson and Bramble, 1993). Second, the length of the upper postcanine row is isometric in D. gliroides, while it is

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TABLE 4 Allometric Comparison of Dromiciops gliroides (this study, multivariate results) with Didelphis albiventris (Abdala et al., 2001) and Lutreolina crassicaudata (Flores et al., 2003)

Variables Dromiciops —_Didelphis __ Lutreolina

Length of nasals + + (-) Height of muzzle (-) = Length of palate = = = Breadth of palate -

Length of upper postcanine row = ~ -

Length of lower postcanine row - - ide

Length of mandible = + = Height of mandible + + + Height of coronoid

process = + = Zygomatic breadth = = 2 Breadth of braincase - _ = Height of occipital

plate - = (-) Length of orbit = a =

Symbols for isometry, negative allometry, and positive allometry are =, -, and +, respectively. Parentheses indicate allometric trends; i.e., situations in which only one of the two regression methods used (least squares and reduced major axis) led to rejection isometry. For instance, in Lutreolina, the length of nasals is negatively allometric under least squares and iso- metric under reduced major axis.

4Value under LS (—), under RMA +.

negative in the didelphids. In fact, D. gliro- ides shows a greatly accentuated trend al- ready present in D. albiventris and L. cras- sicaudata: the upper toothrow elongates much faster than the lower toothrow in order to reach roughly the same length in both rows toward adulthood—a necessary com- pensation because the upper row always bear one tooth less than the lower row until the dentition is completed (Abdala et al., 2001).

In D. albiventris and L. crassicaudata, the breadth of zygoma is isometric and the brain- case width is extremely negatively allometric (Abdala et al., 2001; Flores et al., 2003). Therefore, in relative terms, the space for the temporal muscles increases principally in- wards. The condition in D. gliroides is the same but somewhat less marked, implying that the braincase of young D. gliroides will leave relatively less space to hold the tem- poral muscles. We speculate that this growth pattern may be shared with small-sized Mar-

2004

mosa-like species of marsupials, which have similar braincase size and shape.

CONCLUSIONS

Most of the developmental trends seen in D. gliroides are similar to those found in di- delphids studied so far (Didelphis albiventris and Lutreolina crassicaudata) in spite of the marked size difference, corroborating a com- mon ground of therian development in the sense advanced by Flores et al. (2003) for didelphids (see also Abdala et al., 2001; Maunz and German, 1996). For instance, growth in most neurocranial components were typically negatively allometric, whereas coefficients of splanchnocranial components varied widely in a complex but consistent manner (Abdala et al., 2001; Flores et al., 2003). The six variables that show the same trends in D. gliroides, D. albiventris, and L. crassicaudata define much of the overall shape of the skull, so the three species arrive ontogenetically at their adult proportions in roughly the same way. Other aspects, like the isometry of orbit, development of bulla, and the extremely different allometry shown by the postcanine toothrows, indicate, so far, on- togenetic patterns probably unique to D. gli- roides. An interesting comparison of D. gli- roides’ postnatal ontogeny would be with other small-sized marsupials, both South American and Australasian.

A combination of qualitative observations and allometry continues to provide insightful results in comparative ontogeny of marsupi- als. We found a highly conservative pattern of skull growth in D. gliroides being re- markably similar to that of the two didel- phids studied so far. Inasmuch as D. gliroides is a member of the australidelphian clade, comparisons with didelphids alone are not satisfactory, but this study represents indeed the first ameridelphian-australidelphian com- parison. Therefore, future contributions need to incorporate more australidelphians, for which no data are currently available, in or- der to expand our understanding of the com- parative cranial ontogeny of marsupials as a

group. ACKNOWLEDGMENTS

We are grateful to Guillermo Amico, who provided four specimens prior to their do-

GIANNINI ET AL.: DROMICIOPS GLIROIDES | H,

nation to Centro Regional Universitario Bar- iloche and Colecci6én Mamiferos Lillo, in- cluding the two youngest key specimens of our sample. The following curators and col- lection managers kindly allowed us to study the material for this work: Robert S. Voss (American Museum of Natural History, New York), Rubén M. Barquez (Coleccién Mam- iferos Lillo, Tucumdan), Bruce Patterson (Field Museum of Natural History, Chicago), Ricardo A. Ojeda (Instituto Argentino de In- vestigaciones de Zonas Aridas, Mendoza), Linda Gordon (National Museum of Natural History, Smithsonian Institution, Washing- ton, D.C.), and Olga Vaccaro (Museo Argen- tino de Ciencias Naturales Bernardino Riva- davia). We are thankful to Robert Anderson for his acute and insightful suggestions, and Enrique Guanuco for the great drawings. Robert Voss, Nancy Simmons, and the re- viewers John Wible and Marcelo Sanchez- Villagra contributed significantly to improve this paper. Special thanks to E. Symns and L. Prodan. This work was supported by a Coleman Postdoctoral Research Fellowship from the American Museum of Natural His- tory to N.PG., Limbo Grants Argentina 2001-2002 to N.P.G., a Kalbfleisch Posdoc- toral Research Fellowship from the Ameri- can Museum of Natural History to D.A.F, a Beca de Perfeccionamiento del Consejo de Investigaciones de la Universidad de Tucu- man, Argentina, to D.A.E, and a Postdoctoral Research Fellowship from the University of the Witwatersrand, South Africa, to EA.

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