Craniofacial ontogeny in centrosaurine dinosaurs (Ornithischia: Geratopsidae): taxonomic and behavioral implications

Centrosaurine ceratopsians are characterized by well developed nasal horncores or bosses, relatively abbreviated supraorbital horncores or bosses, and adorned parietosquamosal frills. Recent study of several paucispecific (low diversity) bonebed assemblages in Alberta and Montana has contributed greatly to our understanding of ontogenetic and taxonomic variation in the skulls of centrosaurines. Relative age determination of centrosaurines is now possible through examination of ontogenetic change in several characters, including the surface bone morphology of specific skeletal elements. The within-group taxonomy of centrosaurines is based almost entirely on characters of the skull roof, relating particularly to horns and frills. Juvenile and sub-adult centrosaurines are characterized by relatively simple, unadorned skulls compared to their adult counterparts. As in numerous living taxa, the cranial ornaments of centrosaurines developed late in ontogeny, as individuals approached or attained adult size. An important implication arising directly from this study is that juvenile and sub-adult centrosaurines are difficult to distinguish taxonomically at the specific level. Two monospecific genera represented only by immature materials, Brachyceratops montanensis and Monoclonius crassus , cannot be defended and should be considered nomina dubia . The late ontogenetic development and diverse taxonomic variation of horn and frill morphologies support the contention diat these structures are best interpreted as reproductive characters employed in mate competition.     

Skull ontogeny in Arrhinoceratops brachyops (Ornithischia: Ceratopsidae) and other horned dinosaurs

Disentangling ontogenetic from interspecific variation is key to understanding biodiversity in the fossil record, yet information on growth in the ceratopsid subfamily Chasmosaurinae is sparse. Here, we describe the partial skull of a juvenile chasmosaurine, attributed to Arrhinoceratops brachyops, within the context of more mature specimens of this species, to better understand the ontogenetic transformations therein. We show that as A. brachyops matured, the postorbital horncores became longer and shifted from a posterior to an anterior inclination, the delta‐shaped frill epiossifications became lower and fused to the underlying frill, and the face became more elongate. In these respects, A. brachyops closely resembled Triceratops, suggesting that these ontogenetic changes may have been common to all long‐horned chasmosaurines. However, an event‐paired cladistic analysis of Chasmosaurinae using a standardized matrix of 24 developmental characters reveals that the relative timing of ontogenetic events in Arrhinoceratops was more like that of Chasmosaurus, particularly in the relatively late reduction in scalloping around the frill margins. Thus, the ontogenetic similarities between Arrhinoceratops and Triceratops appear to be plesiomorphic, partly related to the retention of the elongate postorbital horncores, which are primitive for Ceratopsidae. This study elucidates the otherwise contentious evolutionary relationships of Arrhinoceratops, and highlights the importance of ontogenetic data for resolving phylogenies when morphological data from adults alone are inadequate. © 2015 The Linnean Society of London     

Evidence of Combat in Triceratops

Background

The horns and frill of Triceratops and other ceratopsids (horned dinosaurs) are interpreted variously as display structures or as weapons against conspecifics and predators. Lesions (in the form of periosteal reactive bone, healing fractures, and alleged punctures) on Triceratops skulls have been used as anecdotal support of intraspecific combat similar to that in modern horned and antlered animals. If ceratopsids with different cranial morphologies used their horns in such combat, this should be reflected in the rates of lesion occurrence across the skull.

Methodology/Principal Findings

We used a G-test of independence to compare incidence rates of lesions in Triceratops (which possesses two large brow horns and a smaller nasal horn) and the related ceratopsid Centrosaurus (with a large nasal horn and small brow horns), for the nasal, jugal, squamosal, and parietal bones of the skull. The two taxa differ significantly in the occurrence of lesions on the squamosal bone of the frill (P = 0.002), but not in other cranial bones (P>0.20).

Conclusions/Significance

This pattern is consistent with Triceratops using its horns in combat and the frill being adapted as a protective structure for this taxon. Lower pathology rates in Centrosaurus may indicate visual rather than physical use of cranial ornamentation in this genus, or a form of combat focused on the body rather than the head.     

Torosaurus is not Triceratops: ontogeny in chasmosaurine ceratopsids as a case study in dinosaur taxonomy

Background

In horned dinosaurs, taxonomy is complicated by the fact that the cranial ornament that distinguishes species changes with age. Based on this observation, it has been proposed that the genera Triceratops and Torosaurus are in fact synonymous, with specimens identified as Torosaurus representing the adult form of Triceratops. The hypothesis of synonymy makes three testable predictions: 1) the species in question should have similar geographic and stratigraphic distributions, 2) specimens assigned to Torosaurus should be more mature than those assigned to Triceratops, and 3) intermediates should exist that combine features of Triceratops and Torosaurus. The first condition appears to be met, but it remains unclear whether the other predictions are borne out by the fossil evidence.

Methodology/Principal Findings

We assessed the relative maturity of Torosaurus and Triceratops specimens by coding skulls for characters that vary with maturity, and then using a clustering analysis to arrange them into a growth series. We found that a well-defined sequence of changes exists in horned dinosaurs: development of cranial ornament occurs in juveniles, followed by fusion of the skull roof in subadults, and finally, the epoccipitals, epijugals, and rostral fuse to the skull in adults. Using this scheme, we identified mature and immature individuals of both Torosaurus and Triceratops. Furthermore, we describe the ventral depressions on the frill of Triceratops, and show that they differ in shape and position from the parietal fenestrae of Torosaurus. Thus, we conclude that these structures are not intermediates between the solid frill of Triceratops and the fenestrated frill of Torosaurus.

Conclusions/Significance

Torosaurus is a distinct genus of horned dinosaur, not the adult of Triceratops. Our method provides a framework for assessing the hypothesis of synonymy through ontogeny in the fossil record.     

Anatomy and taxonomic status of the chasmosaurine ceratopsid Nedoceratops hatcheri from the upper Cretaceous Lance Formation of Wyoming, U.S.A

Background

The validity of Nedoceratops hatcheri, a chasmosaurine ceratopsid dinosaur known from a single skull recovered in the Lance Formation of eastern Wyoming, U.S.A., has been debated for over a century. Some have argued that the taxon is an aberrant Triceratops, and most recently it was proposed that N. hatcheri represents an intermediate ontogenetic stage between “young adult” and “old adult” forms of a single taxon previously split into Triceratops and Torosaurus.

Methodology/Principal Findings

The holotype skull of Nedoceratops hatcheri was reexamined in order to map reconstructed areas and compare the specimen with other ceratopsids. Although squamosal fenestrae are almost certainly not of taxonomic significance, some other features are unique to N. hatcheri. These include a nasal lacking a recognizable horn, nearly vertical postorbital horncores, and relatively small parietal fenestrae. Thus, N. hatcheri is tentatively considered valid, and closely related to Triceratops spp. The holotype of N. hatcheri probably represents an “old adult,” based upon bone surface texture and the shape of the horns and epiossifications on the frill. In this study, Torosaurus is maintained as a genus distinct from Triceratops and Nedoceratops. Synonymy of the three genera as ontogenetic stages of a single taxon would require cranial changes otherwise unknown in ceratopsids, including additions of ossifications to the frill and repeated alternation of bone surface texture between juvenile and adult morphotypes.

Conclusions/Significance

Triceratops, Torosaurus, and likely Nedoceratops, are all distinct taxa, indicating that species richness for chasmosaurine ceratopsids in the Lance Formation just prior to the Cretaceous-Paleocene extinction was roughly equivalent to that earlier in the Cretaceous.     

An Immature Pachyrhinosaurus perotorum (Dinosauria: Ceratopsidae) Nasal Reveals Unexpected Complexity of Craniofacial Ontogeny and Integument in Pachyrhinosaurus

A new specimen attributable to an immature individual of Pachyrhinosaurus perotorum (Dinosauria, Ceratopsidae) from the Kikak-Tegoseak Quarry in northern Alaska preserves a mix of features that provides refinement to the sequence of ontogenetic stages and transformations inferred for the development of the nasal boss in Pachyrhinosaurus. The new specimen consists of an incomplete nasal that includes the posterior part of the nasal horn, the dorsal surface between the horn and the left-side contacts for the prefrontal and frontal, and some of the left side of the rostrum posteroventral to the nasal horn. The combination of morphologies in the new specimen suggests either an additional stage of development should be recognized in the ontogeny of the nasal boss of Pachyrhinosaurus, or that the ontogenetic pathway of nasal boss development in P. perotorum was notably different from that of P. lakustai. Additionally, the presence of a distinct basal sulcus and the lateral palisade texture on the nasal horn of the specimen described here indicate that a thick, cornified horn sheath was present well before the formation of a dorsal cornified pad. A separate rugose patch on the nasal well posterior to the nasal horn is evidence for a cornified integumentary structure, most likely a thick cornified pad, on the posterior part of the nasal separate from the nasal horn prior to the onset of nasal boss formation in P. perotorum.     

Males Resemble Females: Re-Evaluating Sexual Dimorphism in Protoceratops andrewsi (Neoceratopsia,Protoceratopsidae)

BackgroundProtoceratops andrewsi (Neoceratopsia, Protoceratopsidae) is a well-known dinosaur from the Upper Cretaceous of Mongolia. Some previous workers hypothesized sexual dimorphism in the cranial shape of this taxon, using qualitative and quantitative observations. In particular, width and height of the frill as well as the development of a nasal horn have been hypothesized as potentially sexually dimorphic.Conclusions/SignificanceSexual dimorphism within Protoceratops andrewsi is not strongly supported by our results, as previously proposed by several authors. Anatomical traits such as height and width of the frill, and skull size thus may not be sexually dimorphic. Based on PCA for a data set focusing on the rostrum and associated ANOVA results, nasal horn height is the only feature with potential dimorphism. As a whole, most purported dimorphic variation is probably primarily the result of ontogenetic cranial shape changes as well as intraspecific cranial variation independent of sex.     

Susceptibility to disease varies with ontogeny and immunocompetence in a threatened amphibian

Ontogenetic changes in disease susceptibility have been demonstrated in many vertebrate taxa, as immature immune systems and limited prior exposure to pathogens can place less developed juveniles at a greater disease risk. By causing the disease chytridiomycosis, Batrachochytrium dendrobatidis (Bd) infection has led to the decline of many amphibian species. Despite increasing knowledge on how Bd varies in its effects among species, little is known on the interaction between susceptibility and development within host species. We compared the ontogenetic susceptibility of post-metamorphic green and golden bell frogs Litoria aurea to chytridiomycosis by simultaneously measuring three host-pathogen responses as indicators of the development of the fungus—infection load, survival rate, and host immunocompetence—following Bd exposure in three life stages (recently metamorphosed juveniles, subadults, adults) over 95 days. Frogs exposed to Bd as recently metamorphosed juveniles acquired higher infection loads and experienced lower immune function and lower survivorship than subadults and adults, indicating an ontogenetic decline in chytridiomycosis susceptibility. By corresponding with an intrinsic developmental maturation in immunocompetence seen in uninfected frogs, we suggest these developmental changes in host susceptibility in L. aurea may be immune mediated. Consequently, the physiological relationship between ontogeny and immunity may affect host population structure and demography through variation in life stage survival, and understanding this can shape management targets for effective amphibian conservation.     

Variation in the ontogenetic allometry of horn length in bovids along a body mass continuum

Allometric relationships describe the proportional covariation between morphological, physiological, or life‐history traits and the size of the organisms. Evolutionary allometries estimated among species are expected to result from species differences in ontogenetic allometry, but it remains uncertain whether ontogenetic allometric parameters and particularly the ontogenetic slope can evolve. In bovids, the nonlinear evolutionary allometry between horn length and body mass in males suggests systematic changes in ontogenetic allometry with increasing species body mass. To test this hypothesis, we estimated ontogenetic allometry between horn length and body mass in males and females of 19 bovid species ranging from ca. 5 to 700 kg. Ontogenetic allometry changed systematically with species body mass from steep ontogenetic allometries over a short period of horn growth in small species to shallow allometry with the growth period of horns matching the period of body mass increase in the largest species. Intermediate species displayed steep allometry over long period of horn growth. Females tended to display shallower ontogenetic allometry with longer horn growth compared to males, but these differences were weak and highly variable. These findings show that ontogenetic allometric slope evolved across species possibly as a response to size‐related changes in the selection pressures acting on horn length and body mass.     

Limited flooding tolerance of juveniles restricts the distribution of adults in an understory shrub (Itea virginica; Iteaceae)

Juvenile plants often have tight microhabitat associations because of specific requirements for seed germination and subsequent establishment. Due to their larger size, adults may be more adept at coping with stress. However, few studies consider the role of ontogeny in structuring plant populations, even though phenotypic expression can change through life history. In cypress-tupelo swamps of the United States, understory species often grow on microsites above floodwaters. In a field survey of one such species, Itea virginica, we found that more than 98% of seedlings occurred on elevated microsites, which were relatively infrequent. However, this strict association relaxed through ontogeny, with nearly 8% of subadults and adults rooted directly on the forest floor. We hypothesized that flooding inhibits juvenile establishment on the forest floor. In greenhouse experiments, we investigated the effects of flooding and substrate on Itea performance. Seeds had similar germination rates on drained swamp soil and cypress knee wood. Seedling growth was high on unflooded soil, but declined precipitously when submerged. Finally, performance of seedlings, but not older plants, decreased with flood severity. Our results highlight the importance of assessing stress tolerance over multiple life history stages because limitations of juveniles can constrain the distribution patterns of future ontogenetic stages.     

Ontogenetic habitat preferences of the narrownose smooth-hound shark, Mustelus schmitti, in two Southwestern Atlantic coastal areas

The aim of this study was to determine the ontogenetic habitat preferences of the narrownose smooth-hound shark, Mustelus schmitti, in Río de la Plata and El Rincón coastal areas. There, canonical correspondence analyses of fishery research survey data showed that M. schmitti ontogenetic stages were differentially affected by depth, temperature and salinity. Neonates and juveniles were more abundant and remain in nearshore waters, suggesting the presence of nursery areas in which food availability and environmental conditions allow a faster growth. Adults M. schmitti presented different environmental associations mainly associated with depth and temperature. During non-reproductive season they were associated with deeper coastal waters. With the arrival of the reproductive season, adults migrate from deep to nearshore waters and show sexual segregation associated with pre- or post-mating behaviors. Hence, the year-round presence of neonates and juveniles and the seasonal occurrence of adults in nearshore waters make this habitat essential to M. schmitti population dynamics since key ontogenetic stages will be vulnerable if a direct impact occurs there.     

New observations on the skull of Archaeopteryx

Although skeletal remains of the iconic oldest known avialian Archaeopteryx have been known for almost 150 years, several aspects of the cranial anatomy of this taxon have remained enigmatic, mainly because of the strongly flattened and often fractured and incomplete nature of available skull materials. New investigation of the skulls of the recently described, excellently preserved tenth (Thermopolis) and the seventh (Munich) specimens revealed several previously unrecognized characters and helps to resolve some problematic issues. Thus, the nasal of Archaeopteryx shows a lateral notch for the lacrimal, as is found in many other saurischian dinosaurs, the maxilla clearly participates in the margin of the external nares, and there seems to be a pneumatic foramen in the lacrimal, comparable to the lacrimal fenestra found in many non-avian theropods. In the braincase, Archaeopteryx shows pneumatic features reminiscent of non-avian theropods, including a ventral basisphenoid recess and an anterior tympanic recess that is laterally incised into the basisphenoid/prootic. Most importantly, however, the postorbital process of the jugal shows a facet for the suture with the postorbital, thus resolving the question of whether Archaeopteryx had a closed postorbital bar. A new reconstruction of the skull of Archaeopteryx is presented, making the skull of this taxon even more theropod-like than previously recognized. Furthermore, the closed postorbital bar and the configuration of the bones of the skull roof cast serious doubt on claims that an avian-style cranial kinesis was present in this taxon.     

Temporal consistency of ontogenetic shifts in habitat use by coral reef fishes in the northernmost coral ecosystem in the world (Kudaka Island, Japan)

The prevalence of major habitat shifts in tropical fishes between juvenile and adult stages (ontogenetic shifts) in one of the northernmost coral reefs in the world (Kudaka Island, Japan) is given. The comparative analysis of spatial distribution of juveniles v . adults highlighted four ontogenetic patterns: no change in habitat use between juveniles and adults (five species), a decrease in the number of habitats used by adults compared to juveniles (three species), an increase in the number of habitats used during the adult stage (four species) and use of nursery areas by juveniles followed by extensive movements to different adult habitats (three species). The comparative analysis of fish distribution over time ( i.e. during three consecutive settlement months) showed that 84% of species had temporal consistency in ontogenetic patterns of habitat use.     

Morphology and function of the head in foetal and juvenile Scolecomorphus kirkii (Amphibia: Gymnophiona: Scolecomorphidae)

The external and musculoskeletal morphology of the head is described for an ontogenetic series of the scolecomorphid caecilian Scolecomorphus kirkii . The rostral region of foetuses and juveniles is expanded into large, posterolaterally pointing paraoral processes that are formed by the maxilla. Extraoral teeth are present on the underside of the rostrum and laterally on the paraoral processes. In the foetuses, teeth are covered by epidermal tissue. The endoskeletal part of the foetal skull is largely cartilaginous, but all of the dermal bones, with the exception of the squamosal, are present. The foetal chondrocranium is extensively developed and shows a peculiar, posterolateral process of the nasal capsule that is connected to the trabecula cranii by a transverse bar posterior to the choana, and extends further posterior beyond the level of the posterior end of the pila antotica. Only two mm. adductor mandibulae are present, together with two pterygoideus muscles that insert onto the lower jaw. The palatoquadrate and quadrate of foetuses and juveniles, respectively, are highly mobile. It is suggested that the derived head morphology of Scolecomorphus foetuses and juveniles is an adaptation to specialized postparitive feeding.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 491–504.     

Size and growth characteristics of dispersing voles,Microtus townsendii

Summary In a peak population of Microtus townsendii, adults and subadults dispersed during the spring decline, and subadults and juveniles dispersed during the summer and fall. Voles born in the spring dispersed before the start of the next year's breeding season, whereas fall-born voles dispersed during the next year's breeding season. Voles under 50 g, when they dispersed, had faster growth rates than similar-sized residents, but voles over 59 g, when they dispersed, had slower growth rates than similar-sized residents. Dispersing and resident voles 50–59 g had no consistent trend in growth rates.     

Cranial ontogenetic variability,sex ratio and age structure of the Red fox

Describing the sex ratio, age structure of the population and ontogenetic variability of Red fox, Vulpes vulpes (Canidae, Carnivora) skull parameters, this study is based on 416 male and 289 female skulls collected in the Czech Republic. The skulls analysed came from feral individuals, that were shot by hunters. The male to female ratio was 1:0.69 regarding the whole population. Individuals younger than one year prevailed in the population (54% males, 48% females were in their first year of life). Four growth patterns of skull dimensions were described. The first group included mainly skull length dimensions (e.g. condylobasal length). They grew rapidly until the sixth month of life, becoming stabilised afterwards. The second group comprised parameters that were stable throughout the life (e.g. cheek tooth rows). Measurements representing the third growth pattern showed continual growth (mainly width dimensions, e.g. zygomatic breadth). Conversely, smaller dimensions of postorbital breadth were observed after the sixth month of life. Postorbital breadth represented the fourth growth pattern. It was concluded, that male and female Red foxes had similar ontogenetic skull development, even though there were some differences, e.g. in jugular breadth, which increased after the age of six months in males unlike in females.     

Ontogeny of cranial ossification in the eastern newt, Notophthalmus viridescens (Caudata: Salamandridae), and its relationship to metamorphosis and neoteny

The ontogenetic sequence of cranial osteogenesis through adulthood is described in samples of newts from completely metamorphosing and partially neotenic populations. Cranial ossification proceeds in the same sequence in both samples. Seven stages of cranial development are described on the basis of conspicuous events that occur during ontogeny. These include four larval stages, metamorphs, efts, and adults. Neotenic adults have skulls that are metamorphosed completely and indistinguishable from the skulls of non-neotenic adults. Neoteny in these newts does not involve the skull and is limited to the postmetamorphic retention of some gill structures and, thus, is termed "limited neoteny." The evolution of limited neoteny in newts as a correlated response to the inhibition of land-drive behavior is discussed.     

Allometry and developmental integration of body growth in a piranha,Pygocentrus nattereri (Teleostei: Ostariophysi)

Piranhas, like many teleosts, change their diets on both ontogenetic and phylogenetic time scales. Prior studies have suggested that pervasive morphological changes in body form on a phylogenetic time scale may be related to changes in diet, but previous reports have found little shape change in piranhas on an ontogenetic time scale. We re-examine the post-transformational allometry of body form in one piranha, Pygocentrus nattereri (Kner), using the method of thin-plate splines decomposed by their partial warps. We find substantial evidence of allometry, primarily elongation of the mid-body relative to the more anterior and posterior regions, elongation of the postorbital and nape regions relative to the more anterior head and posterior body, and deepening of the head relative to the body. In addition to these pervasive changes throughout the body, there are some that are more localized, especially elongation of the postorbital region relative to eye diameter and snout, and an even more localized elongation of the snout relative to eye diameter. Initial dietary transitions are associated with changes in head and jaw proportions, but rates of shape change decelerate through growth, so that the final transition to a diet increasingly dominated by small whole fish appears associated with change largely in overall body size. © 1995 Wiley-Liss, Inc.     

Cranial asymmetry in a Dall sheep ram (Ovis dalli dalli).

The horns of a 13-yr-old Dall sheep ram (Ovis dalli dalli) from the Sheep Mountain herd in Kluane National Park (Yukon, Canada) had unique characteristics. The right horn was 1,127 mm long, while the left horn was only 861 mm long and compressed and distorted at its base. The reduced growth of the left horn was due to chronic epidermitis and osteomyelitis of the cornual process, which began when the ram was 5 yr of age.     

Heterogeneity in male horn growth and longevity in a highly sexually dimorphic ungulate

In sexually dimorphic ungulates, sexual selection favoring rapid horn growth in males may be counterbalanced by a decrease in longevity if horns are costly to produce and maintain. Alternatively, if early horn growth varied with individual quality, it may be positively correlated with longevity. We studied Alpine ibex Capra ibex in the Gran Paradiso National Park, Italy, to test these alternatives by comparing early horn growth and longevity of 383 males that died from natural causes. After accounting for age at death, total horn length after age 5 was positively correlated with horn growth from two to four years. Individuals with the fastest horn growth as young adults also had the longest horns later in life. Annual horn growth increments between two and six years of age were independent of longevity for ibex whose age at death ranged from 8 to 16 years. Our results suggest that growing long horns does not constrain longevity. Of the variability in horn length, 22% could be explained by individual heterogeneity, suggesting persistent differences in phenotypic quality among males. Research on unhunted populations of sexually dimorphic ungulates documents how natural mortality varies according to horn or antler size, and can help reduce the impact of sport hunting on natural processes.