The Functional Morphology of Avicularia in Cheilostome Bryozoans

<p>Avicularia are modified zooids characteristic of cheilostome bryozoans. Through evolutionary time the functional capacity of the polypide has evolved and is now a vestigial feature within the avicularium. The functional role of avicularia in the colony is unclear. Unable to feed, avicularia are dependent on nutrients from the parental or neighbouring zooids and therefore constitute a significant metabolic cost in production and maintenance, a cost which must be met by some reciprocal function. Details on the functional morphology of avicularia are severely lacking with avicularia constituting a large gap in the knowledge of cheilostome biology. By examining their biology, this study will enhance our understanding of the evolution and functional capacity of avicularia. Fundamentally this study will provide insight into the degree of morphological and morphometric divergence among avicularia. The objective of this study was to: (1) conduct a morphological survey of the putative sensory structures associated with the palate (or orificial structures) of avicularia (SEM); (2) conduct an ultrastructural-level study (TEM) of the vestigial polypide from two species of bugulids from disparate habitats; and (3) incorporate a holistic study on the behaviour and functional evolution of character traits in Bugula flabellata. The avicularia from 38 species of cheilostome bryozoans were examined covering 11 superfamilies, 18 families and 29 genera. The results indicate that avicularia are morphologically diverse and display extensive variation in avicularian orifice morphology. Structures associated with the orifice varied from tufts of cilia, simple pores, tubular protuberances, and pores with an organic exude. The adventitious avicularia dominated (83%) and displayed the greatest morphometric diversity compared with interzooidal, vicarious and vibracular types. Within superfamilies, only the catenicellids displayed a significant level of morphometric and anatomical congruence. The density of avicularia within a colony was greatest by combining adventitious and vibracular types (e.g. Caberea). This finding may represent an evolutionary shift towards maximisation of function within a smaller spatial scale. The ultrastructure of the vestigial polypide of the subtidal B. flabellata and deep-sea Nordgaardia cornucopioides revealed disparities suggestive of differing functional roles either as a result of habitat differences or differing stages of evolutionary development. The avicularium of B. flabellata has undergone significant modification in character traits from the plesiomorphic autozooid. The current anatomy and behaviour of this avicularium provides strong evidence for a mechanoreceptive function whereby detection of tactile stimuli from passing invaders is important in the functional role of the bird's-head avicularium of B. flabellata. This study is the first to examine the functional morphology of avicularia in such detail. The techniques used in this study have never been applied to avicularia before allowing numerous features such as the muscles, orificial structures and vestigial polypide anatomy to be discerned. The results indicate that avicularia are morphologically diverse and anatomically equipped to perform a variety of functions. The morphological diversity of avicularia may be of immense ecological importance and represent differing responses to various selective pressures in the environment.</p>

The Functional Morphology of Avicularia in Cheilostome Bryozoans

<p>Avicularia are modified zooids characteristic of cheilostome bryozoans. Through evolutionary time the functional capacity of the polypide has evolved and is now a vestigial feature within the avicularium. The functional role of avicularia in the colony is unclear. Unable to feed, avicularia are dependent on nutrients from the parental or neighbouring zooids and therefore constitute a significant metabolic cost in production and maintenance, a cost which must be met by some reciprocal function. Details on the functional morphology of avicularia are severely lacking with avicularia constituting a large gap in the knowledge of cheilostome biology. By examining their biology, this study will enhance our understanding of the evolution and functional capacity of avicularia. Fundamentally this study will provide insight into the degree of morphological and morphometric divergence among avicularia. The objective of this study was to: (1) conduct a morphological survey of the putative sensory structures associated with the palate (or orificial structures) of avicularia (SEM); (2) conduct an ultrastructural-level study (TEM) of the vestigial polypide from two species of bugulids from disparate habitats; and (3) incorporate a holistic study on the behaviour and functional evolution of character traits in Bugula flabellata. The avicularia from 38 species of cheilostome bryozoans were examined covering 11 superfamilies, 18 families and 29 genera. The results indicate that avicularia are morphologically diverse and display extensive variation in avicularian orifice morphology. Structures associated with the orifice varied from tufts of cilia, simple pores, tubular protuberances, and pores with an organic exude. The adventitious avicularia dominated (83%) and displayed the greatest morphometric diversity compared with interzooidal, vicarious and vibracular types. Within superfamilies, only the catenicellids displayed a significant level of morphometric and anatomical congruence. The density of avicularia within a colony was greatest by combining adventitious and vibracular types (e.g. Caberea). This finding may represent an evolutionary shift towards maximisation of function within a smaller spatial scale. The ultrastructure of the vestigial polypide of the subtidal B. flabellata and deep-sea Nordgaardia cornucopioides revealed disparities suggestive of differing functional roles either as a result of habitat differences or differing stages of evolutionary development. The avicularium of B. flabellata has undergone significant modification in character traits from the plesiomorphic autozooid. The current anatomy and behaviour of this avicularium provides strong evidence for a mechanoreceptive function whereby detection of tactile stimuli from passing invaders is important in the functional role of the bird's-head avicularium of B. flabellata. This study is the first to examine the functional morphology of avicularia in such detail. The techniques used in this study have never been applied to avicularia before allowing numerous features such as the muscles, orificial structures and vestigial polypide anatomy to be discerned. The results indicate that avicularia are morphologically diverse and anatomically equipped to perform a variety of functions. The morphological diversity of avicularia may be of immense ecological importance and represent differing responses to various selective pressures in the environment.</p>

When fossil clades ‘compete’: local dominance, global diversification dynamics and causation

Examining the supposition that local-scale competition drives macroevolutionary patterns has become a familiar goal in fossil biodiversity studies. However, it is an elusive goal, hampered by inadequate confirmation of ecological equivalence and interactive processes between clades, patchy sampling, few comparative analyses of local species assemblages over long geological intervals, and a dearth of appropriate statistical tools. We address these concerns by reevaluating one of the classic examples of clade displacement in the fossil record, in which cheilostome bryozoans surpass the once dominant cyclostomes. Here, we analyse a newly expanded and vetted compilation of 40 190 fossil species occurrences to estimate cheilostome and cyclostome patterns of species proportions within assemblages, global genus richness and genus origination and extinction rates while accounting for sampling. Comparison of time-series models using linear stochastic differential equations suggests that inter-clade genus origination and extinction rates are causally linked to each other in a complex feedback relationship rather than by simple correlations or unidirectional relationships, and that these rates are not causally linked to changing within-assemblage proportions of cheilostome versus cyclostome species.

A comparative analysis of the nervous system of cheilostome bryozoans

Background Bryozoans are sessile aquatic suspension feeders in mainly marine, but also freshwater habitats. Most species belong to the marine and calcified Cheilostomata. Since this taxon remains mostly unstudied regarding its neuroanatomy, the focus of this study is on the characterization and ground pattern reconstruction of the autozooidal nervous system based on six representatives. Results A common neuronal innervation pattern is present in the investigated species: a cerebral ganglion is located at the base of the lophophore, from where neurite bundles embrace the mouth opening to form a circumoral nerve ring. Four neurite bundles project from the cerebral ganglion to innervate peripheral areas, such as the body wall and parietal muscles via the tentacle sheath. Five neurite bundles comprise the main innervation of the visceral tract. Four neurite bundles innervate each tentacle via the circumoral nerve ring. Mediofrontal tentacle neurite bundles emerge directly from the nerve ring. Two laterofrontal- and one abfrontal tentacle neurite bundles emanate from radial neurite bundles, which originate from the cerebral ganglion and circumoral nerve ring in between two adjacent tentacles. The radial neurite bundles terminate in intertentacular pits and give rise to one abfrontal neurite bundle at the oral side and two abfrontal neurite bundles at the anal side. Similar patterns are described in ctenostome bryozoans. Conclusions The present results thus represent the gymnolaemate situation. Innervation of the tentacle sheath and visceral tract by fewer neurite bundles and tentacular innervation by four to six tentacle neurite bundles support cyclostomes as sister taxon to gymnolaemates. Phylactolaemates feature fewer distinct neurite bundles in visceral- and tentacle sheath innervation, which always split in nervous plexus, and their tentacles have six neurite bundles. Thus, this study supports phylactolaemates as sistergroup to myolaemates.

A broadly resolved molecular phylogeny of New Zealand cheilostome bryozoans as a framework for hypotheses of morphological evolution

Larger molecular phylogenies based on ever more genes are becoming commonplace with the advent of cheaper and more streamlined sequencing and bioinformatics pipelines. However, many groups of inconspicuous but no less evolutionarily or ecologically important marine invertebrates are still neglected in the quest for understanding species- and higher-level phylogenetic relationships. Here, we alleviate this issue by presenting the molecular sequences of 165 cheilostome bryozoan species from New Zealand waters. New Zealand is our geographic region of choice as its cheilostome fauna is taxonomically, functionally and ecologically diverse, and better characterized than many other such faunas in the world. Using this most taxonomically broadly-sampled and statistically-supported cheilostome phylogeny comprising 214 species, when including previously published sequences, we tested several existing systematic hypotheses based solely on morphological observations. We find that lower taxonomic level hypotheses (species and genera) are robust while our inferred trees did not reflect current higher-level systematics (family and above), illustrating a general need for the rethinking of current hypotheses. To illustrate the utility of our new phylogeny, we reconstruct the evolutionary history of frontal shields (i.e., a calcified bodywall layer in ascus-bearing cheilostomes) and asked if its presence has any bearing on the diversification rates of cheilostomes.

Are local dominance and inter-clade dynamics causally linked when one fossil clade displaces another?

Disputing the supposition that ecological competition drives macroevolutionary patterns is now a familiar goal in many fossil biodiversity studies. But it is an elusive goal, hampered by patchy sampling, few assemblage-level comparative analyses, unverified ecological equivalence of clades and a dearth of appropriate statistical tools. We address these concerns with a fortified and vetted compilation of 40190 fossil species occurrences of cyclostome and cheilostome bryozoans, a canonical example of one taxonomically dominant clade being displaced by another. Dramatic increases in Cretaceous cheilostome genus diversification rates begin millions of years before cheilostomes overtake cyclostomes in local species proportions. Moreover, analyses of origination and extinction rates over 150 Myr suggest that inter-clade dynamics are causally linked to each other, but not to changing assemblage-level proportions.One Sentence SummaryGlobal fossil diversification rates and local taxonomic dominance are not causally linked.

Erect bifoliate species of Microporella (Bryozoa, Cheilostomata), fossil and modern

Microporella Hincks, 1877 is one of the most diverse genera of cheilostome bryozoans, containing more than 150 named species. Distributed globally since the early Miocene, the majority of species of Microporella have sheet-like colonies encrusting hard and / or ephemeral substrates, while a limited number of species have erect bifoliate colonies starting from an encrusting base. Herein, the four nominal species of erect bifoliate Microporella (M. bifoliata, M. hastigera, M. hyadesi and M. ordo) are revised, and one new Pliocene (M. tanyae sp. nov.) and three new Recent species (M. ordoides sp. nov., M. lingulata sp. nov. and M. modesta sp. nov.) are formally described. Furthermore, the lectotype and paralectotypes were designated for M. bifoliata and M. hastigera. An additional Recent species, Microporella sp. 1, is also described and illustrated but left in open nomenclature owing to the absence of ovicells in the single available fragment. Although the molecular phylogeny of Microporella has yet to be resolved, the diversity of character states present among the erect bifoliate species described here suggests that this colony growth-form is not monophyletic but has evolved on multiple occasions.

A radical, novel design for a free-living bryozoan colony: Biselenaria placentula (Reuss, 1867)

A series of well-preserved specimens of the little-known Palaeogene species Biselenaria placentula (Reuss, 1867) warrant the designation of a new family of free-living cheilostome bryozoans, Biselenariidae n. fam. In contrast to the structural organization of all other free-living, lunulitiform cheilostomes, all zooids are enclosed almost completely by cuticular, exterior walls. Yet, like other lunulitiforms, the colony must be regarded as a highly integrated functional unit, as revealed through the unique, highly complex interior architecture. In creating the new monotypic family, the type species Biselenaria placentula is described in detail, while the ambiguous taxonomic status of the only other taxon, B. offa Gregory, 1893, is discussed.UUID: http://zoobank.org/6ad8a795-c45e-4619-b2bb-46916585fbd9