skip to main content


Title: Ontogenetic variation in the ecological stoichiometry of 10 fish species during early development
Abstract

The chemical composition and stoichiometry of vertebrate bodies changes greatly during ontogeny as phosphorus‐rich bones form, but we know little about the variation among species during early development. Such variation is important because element ratios in animal bodies influence which element limits growth and how animals contribute to nutrient cycling. We quantified ontogenetic variation from embryos through 2–3 months of age in 10 species of fish in six different families, ranging in adult size from 73 to 720 mm in length. We measured whole‐body concentrations (percentage of dry mass) and ratios of carbon (C), nitrogen (N), and phosphorus (P) as fish developed. We also quantified whole‐body concentrations of calcium (Ca), because Ca should reflect bone development, and RNA, which can be a major pool of body P. To account for interspecific differences in adult size, we also examined how trends changed with relative size, defined as body length divided by adult length. Ontogenetic changes in body composition and ratios were relatively similar among species and were more similar when expressed as a function of relative size compared to age. Body P increased rapidly in all species (likely because of bone development) from embryos until individuals were ~5%–8% of adult size. Body N also increased, while body C, C:N, C:P, and N:P all decreased over this period. Body Ca increased with development but was more variable among species. Body RNA was low in embryos, increased rapidly in young larvae, then decreased as fish reached 5%–8% of adult size. After fish were about 5%–8% of adult size, changes in body composition were relatively slight for all elements and ratios. These results reveal a consistency in the dynamics of body stoichiometry during early ontogeny, presumably because of similar constraints on the allocation of elements to bones and other body pools. Because most changes occur when individuals are <1 month old (<10% of adult size for that species), early ontogenetic variation in body stoichiometry may be especially important for growth limitation of individuals and ecosystem‐level nutrient cycling.

 
more » « less
NSF-PAR ID:
10470022
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology
Volume:
104
Issue:
12
ISSN:
0012-9658
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Trabecular bone structure in adulthood is a product of a process of modelling during ontogeny and remodelling throughout life. Insight into ontogeny is essential to understand the functional significance of trabecular bone structural variation observed in adults. The complex shape and loading of the human calcaneus provides a natural experiment to test the relationship between trabecular morphology and locomotor development. We investigated the relationship between calcaneal trabecular bone structure and predicted changes in loading related to development of gait and body size in growing children. We sampled three main trabecular regions of the calcanei using micro‐computed tomography scans of 35 individuals aged between neonate to adult from the Norris Farms #36 site (1300 AD, USA) and from Cambridge (1200–1500 AD, UK). Trabecular properties were calculated in volumes of interest placed beneath the calcaneocuboid joint, plantar ligaments, and posterior talar facet. At birth, thin trabecular struts are arranged in a dense and relatively isotropic structure. Bone volume fraction strongly decreases in the first year of life, whereas anisotropy and mean trabecular thickness increase. Dorsal compressive trabecular bands appear around the onset of bipedal walking, although plantar tensile bands develop prior to predicted propulsive toe‐off. Bone volume fraction and anisotropy increase until the age of 8, when gait has largely matured. Connectivity density gradually reduces, whereas trabeculae gradually thicken from birth until adulthood. This study demonstrates that three different regions of the calcaneus develop into distinct adult morphologies through varying developmental trajectories. These results are similar to previous reports of ontogeny in human long bones and are suggestive of a relationship between the mechanical environment and trabecular bone architecture in the human calcaneus during growth. However, controlled experiments combined with more detailed biomechanical models of gait maturation are necessary to establish skeletal markers linking growth to loading. This has the potential to be a novel source of information for understanding loading levels, activity patterns, and perhaps life history in the fossil record.

     
    more » « less
  2. Zebrafish are a valuable model for normal vertebrate skeletogenesis and the study of myriad bone disorders. Bones grow, ossify and change shape throughout the zebrafish lifetime, and 3D technologies allow us to examine skeletogenic processes in detail through late developmental stages. To facilitate analysis of shape, orientation and tissue density of skeletal elements throughout ontogeny and adulthood, we generated a high-resolution skeletal reference dataset of wild-type zebrafish development. Using microCT technology, we produced 3D models of the skeletons of individuals ranging from 12 to 25 mm standard length (SL). We analyzed the dynamics of skeletal density and volume as they increase during juvenile and adult growth. Our resource allows anatomical comparisons between meristic units within an individual—e.g., we show that the vertebral canal width increases posteriorly along the spine. Further, structures may be compared between individuals at different body sizes: we highlight the shape changes that the lower jaw undergoes as fish mature from juvenile to adult. We show that even reproductively mature adult zebrafish (17–25 mm SL) continue to undergo substantial changes in skeletal morphology and composition with continued adult growth. We provide a segmented model of the adult skull and a series of interactive 3D PDFs at a range of key stages. These resources allow changes in the skeleton to be assessed quantitatively and qualitatively through late stages of development, and can serve as anatomical references for both research and education. 
    more » « less
  3. Abstract

    Archosauromorph reptiles underwent rapid lineage diversification, increases in morphological and body size disparity, and expansion into new adaptive landscapes. Several of the primary early archosauromorph clades (e.g. rhynchosaurs) are easy to differentiate from others because of their characteristic body types, whereas the more lizard‐like and carnivorous forms with long necks (e.g. tanystropheids) were historically all relegated to the groups Protorosauria or Prolacertiformes. However, it is now clear that these groups are polyphyletic and that a lizard‐like, carnivorous form is plesiomorphic for Archosauromorpha, and multiple subclades started with that body plan. Among these early forms isMalerisaurusfrom the Upper Triassic of India (M. robinsonae) and the Upper Triassic of south‐western USA (M. langstoni). In this paper, we critically re‐evaluate the genus. We find both species ofMalerisaurusas valid, and identifyMalerisaurusas an early diverging, but late‐surviving, carnivorous member of Azendohsauridae within Allokotosauria. Our histological analysis and assessment of ontogenetic changes of limb bones of small and large individuals demonstrate that the skeletons of the small forms grew slowly and became more robust through ontogeny, and that the larger recovered bones are at or near the maximum size of the taxon.MalerisaurusandMalerisaurus‐like taxa were common members of the Otischalkian–Adamanian (late Carnian to mid‐Norian) faunal assemblages from Upper Triassic strata of the south western USA, but they are absent from the younger Revueltian holochronozone. Specimens from western North America show that Allokotosauria had a near‐Pangaean distribution for much of the Middle Triassic to Late Triassic.

     
    more » « less
  4. null (Ed.)
    The rise of mammals after the extinction of the dinosaurs remains one of the most enigmatic intervals in the evolution of mammals. A relatively sparse Paleocene fossil record and confusing interrelationships between taxa means that little is known of the evolution, ecology, and biology of these animals. As a result, the life history of these organisms is completely unstudied, despite likely playing a key role in the ability of these clades to rapidly proliferate and increase in body size in recovering ecosystems. However, intensive collection efforts in the San Juan Basin of New Mexico in the last decade have drastically improved the record of many Paleocene mammals, and offer the first opportunity to address questions about the life history of these animals. Here, we present preliminary results of an in-depth paleohistological analysis of Pantolambda bathmodon, an early, possibly gregarious pantodont, using an ontogenetic series of individuals. Pantodonts were bizarre, herbivorous eutherians of unknown phylogenetic affinity, and were among the first mammal lineages to reach large body sizes in the Paleocene. In examining both dental and skeletal records of growth from the same individuals, including a juvenile still bearing deciduous teeth, our study is among the most comprehensive paleohistological analyses of any fossil mammal. This intensive approach allows for unprecedented insights into the life history of this species. Neonatal lines in the teeth indicate that the deciduous premolars and the first upper molar were erupted prior to birth, similar to precocious, nidifugous mammals today. Daily incremental lines in the enamel and dentine suggest rapid crown formation times (~45–70 days) and a gestation period of at least 15 weeks. A stress line in the postcranial bones, recording an anomalous decrease in growth towards the end of this individual’s life, may represent the weaning event. In the absence of geochemical evidence, it is unclear which of two stress lines in the teeth corresponds to this event, but these lines occur roughly one and two months after birth, respectively. The weanling perished approximately 2.5 months after birth, weighing about 17 kg. An adult individual exhibiting severe wear on the dentition allows us to estimate maximum longevity in Pantolambda bathmodon at about 7 years. In comparison with life history data on living mammals from the PanTheria dataset, Pantolambda bathmodon had a gestation length and weaning duration below average for a placental of its adult body size (42 kg), but within the range of known variation. However, its lifespan was exceptionally short, falling outside the bounds of comparable living mammals. Together, these lines of evidence suggest a relatively rapid pace of life in Pantolambda bathmodon, despite its relatively large body size. Ongoing sampling of more individuals and geochemical analyses should allow for estimation of time to sexual maturity and help to confirm the identity of the weaning line, completing our picture of the life history of this pioneering species. 
    more » « less
  5. Abstract Objectives

    The effects of phylogeny and locomotor behavior on long bone structural proportions are assessed through comparisons between adult and ontogenetic samples of extant gorillas.

    Materials and Methods

    A total of 281 wild‐collected individuals were included in the study, divided into four groups that vary taxonomically and ecologically: western lowland gorillas (G. g. gorilla), lowland and highland grauer gorillas(G. b. graueri), and Virunga mountain gorillas (G. b. beringei). Lengths and articular breadths of the major long bones (except the fibula) were measured, and diaphyseal cross‐sectional geometric properties determined using computed tomography. Ages of immature specimens (n = 145) were known or estimated from dental development. Differences between groups in hind limb to forelimb proportions were assessed in both adults and during development.

    Results

    Diaphyseal strength proportions among adults vary in parallel with behavioral/ecological differences, and not phylogeny. The more arboreal western lowland and lowland grauer gorillas have relatively stronger forelimbs than the more terrestrial Virunga mountain gorillas, while the behaviorally intermediate highland grauer gorillas have intermediate proportions. Diaphyseal strength proportions are similar in young infants but diverge after 2 years of age in western lowland and mountain gorillas, at the same time that changes in locomotor behavior occur. There are no differences between groups in length or articular proportions among either adults or immature individuals.

    Conclusion

    Long bone diaphyseal strength proportions in gorillas are developmentally plastic, reflecting behavior, while length and articular proportions are much more genetically canalized. These findings have implications for interpreting morphological variation among fossil taxa.

     
    more » « less