Functional adaptation of spiriferide brachiopod morphology

It has been suggested that spiriferide morphologies have evolved to adapt to a variety of environmental conditions. Through a computational fluid dynamics approach, we examined how the spiriferide original form was optimized for a lotic condition, specifically addressing the functionalization of the Devonian spiriferide brachiopod Paraspirifer bownockeri to generate passive feeding flows. The results using four models, each of which differed in the development of the spiriferide shell depression, i.e. sulcus, showed that a deeper sulcus functions to create strong spiral flows so as to align on the feeding organ inside the shell. Among the sulcus‐developed models, only the mimic of the natural form could generate comparative slow flows with a stable inflow area. The fossil record of spiriferides shows a morphological trade‐off between the development of the sulcus and wing form. We concluded that spiriferide shells with such a morphological combination evolved to produce various feeding strategies, resulting in diversification.     

Computational fluid dynamics simulations on a Devonian spiriferid Paraspirifer bownockeri (Brachiopoda): Generating mechanism of passive feeding flows

A mechanism of generating passive feeding flow for the Devonian spiriferide brachiopod Paraspirifer bownockeri was theoretically elucidated through fluid dynamics simulations for flow around rigid shells. The RANS equations were used as a turbulence model, and the unsteady incompressible flow was solved using the finite volume method. Two directions of ventral and dorsal flows were investigated as typical cases where little exchange flow occurs inside the shells. The digital model of the shell was constructed using image processing of X-ray CT images of a shell replica made by molding a polycarbonate plate to a well-preserved fossil specimen of Paraspirifer. To examine the effect of flow velocity, three conditions of ambient flow velocity were adopted for both the ventral and dorsal flows. The pressure distribution along the gape showed that a relatively high pressure occurred around the sulcus in all simulated cases. This high pressure generated inflow from the sulcus and subsequent spiral internal flow, especially in fast ambient flows. This means that the sulcus generated the considerable pressure gradient around the gape passively and generated the stable intake of seawater and a spiral flow of water inside the shell for feeding. We conclude that the shell form of certain spiriferides could generate spiral flows so as to promote passive feeding, and the sulcus is interpreted as an important form for the passive intake of water.     

Theoretical approach to the functional optimisation of spiriferide brachiopod shell: Optimum morphology of sulcus

Evidence suggests that biological forms that provide physiological and autecological functions have evolved to adapt to environmental conditions and to optimise requisite morpho-functions. We examined whether shell morphology is functionally optimised to generate passive feeding flow in the Devonian spiriferide brachiopod Paraspirifer bownockeri. This study was based on quantitative results from a computational fluid dynamics simulation and the Lagrangian multiplier method. We estimated the optimum development of the ventral median shell depression, which is called the sulcus, by minimising the pressure difference along the gape. This estimation was made under the constraint that the number of spiral flow rotations must be greater than one, which is effective for spiriferide feeding because of its alignment with the spiral lophophore. During mathematical optimisation, the equation resulted in a suitable flow velocity of approximately 0.1 m/s. At this velocity, the pressure difference was minimised, regardless of sulcus development. The constraint equation showed that the number of spiral flow rotations increased with sulcus development. The optimal solution was similar to the original sulcus form of Paraspirifer under an ambient flow of approximately 0.1 m/s. This result suggests that the variation of shell outline in spiriferids could provide a variety of preferential conditions for ambient flow and that the flow intensity could be adjusted by sulcus development to generate a robust passive feeding flow along the spiral feeding organs.     

Hydrodynamic advantages in the free‐living spiriferinide brachiopod Pachycyrtella omanensis: functional insight into adaptation to high‐energy flow environments

Immobile benthic organisms lacking attachment or cementation mechanisms are considered to be best adapted to quiet bottom environments. Since the free‐living Lower Permian spiriferinide brachiopod Pachycyrtella omanensis inhabited a sandy substrate with high‐energy water flow, flume experiments were performed to show the possible hydrodynamic advantages of shell morphology in postural stability and generation of feeding flows. Modelling indicates that a vertical position, with the commissure plane perpendicular to the seabed, was the most unstable, although it is considered to have been its original life position. On the other hand, the passive flow inside the model in vertical position exhibited vortex movement with constant degree of inhalent flow and exhalent flow, conferring advantages on the effective filtration of food particles using a spiral lophophore. The intensity and movement of the passive flow for feeding could have been adjusted through changes in the angle of opening of the valves. As the shoreface habitat was affected by oscillatory flows, a small‐sized animal could have undergone a high risk of burial, while an increase in size would have led to easier removal from the sandy bottom. To avoid both physical risks, Pachycyrtella developed a thick shell with a high rate of growth, specifically increasing the weight of the ventral umbo without altering its morphofunction to generate passive feeding flows. Biomechanics, functional morphology, opportunistic species, Pachycyrtella, Spiriferinida, suspension feeder.     

Changes in the communities of Paleozoic brachiopods due to their development of their filtering system

Onward changes in the communities of Paleozoic articulated brachiopods were mainly connected with the improvement of the function of their filter feeding system, which is responsible for the feeding of animals. Three major routes of improvement are known: (1) feeding using a primitive lophophore and specialized mantle (orders Strophomenida, Chonetida, and Productida); (2) increased complexity and enlargement of the spirolophe and the appearance of the spiral brachidium (orders Atrypida, Spiriferida, and Athyridida); (3) development of the protective structures preventing ingestible particles into the inner cavity of the shell (order Rhynchonellida). The most effective was the third variant that allowed rhynchonellids, which appeared in the Ordovician, to live up to recently and survive after two largest extinctions in the history of the group development: in the Late Devonian and at the Permian-Triassic boundary.     

How does flow recruit epibionts onto brachiopod shells? Insights into reciprocal interactions within the symbiotic framework

Computational fluid dynamics simulations were performed to examine the passive recruitment of epibionts onto Devonian spiriferide brachiopod host shells. Because many planktonic larvae and spores are propulsion-inefficient swimmers, we determined the areas most prone to settlement in terms of inertial impaction and direct interception, which are characteristic of higher and lower pressure, respectively. Simulations on a unique specimen of Paraspirifer with a geopetal structure of broken brachidia suggest that the larva of Aulopora on the shell was transported and had settled onto the shell through inertial impaction after the host was dead and overturned on the sea floor. In the case of an ideal life posture, the spiriferide models received higher pressure on the shell surfaces at the forward and rearward stagnation areas and lower pressure along the shell margins and the anterior part of the sulcus, regardless of whether the ventral or the dorsal valve was facing upstream. Both sites seem to be available for epibionts by way of direct interception or inertial impaction. Our results indicate that the initial recruitment of most epibionts is accidental and passive, whereas the directions and patterns of epibiont growth suggest a biological response to ambient conditions.     

Discovery of ventrally directed spiralia in a Permian spiriferellid brachiopod and implications for its feeding system

Spiralia are lophophore‐supporting, coiled internal structures developed in some extinct brachiopods. In spite of considerable variations in their orientation, the spiralia of most spiriferide and spiriferinide taxa are known to be laterally directed. Recent studies have shown that these brachiopods consistently have a median inhalant and lateral exhalant feeding system. Here, we report a Permian spiriferellid brachiopod fossil (Spiriferella protodraschei) bearing ventrally directed spiralia in its interior. Using the serial sections of the specimen, we have reconstructed the detailed morphology and orientation of the spiralia. Each spiralium in the specimen does not show the apically tapering pattern supposedly universal in all the known types of spiralia: instead it maintains a similar diameter even at its last whorl. The spiralia appear to have directly developed from strong and anteriorly extended crura, consisting of ten whorls in one side and 13 whorls in the other side. As the morphology and orientation of spiralia are immediately associated with the arrangement of spirolophous lophophore within the mantle cavity, the extraordinary orientation and form of the spiralia indicate that this brachiopod likely had developed a considerably modified feeding pattern with respect to most other spirolophous brachiopods. It is postulated that the inhalant/exhalant current circulation of the species (and its descendants) would be considerably different from that of other spiriferide taxa. In particular, the combination of the vertically oriented life posture (free‐lying with thickened ventral apex bottom) and ventrally directed spiralia resembles both fossil atrypide and modern rhynchonellide brachiopods in the orientation of spirolophe, suggesting that some spiriferellid brachiopods may have developed a lateral inhalant/median exhalant feeding current system. A few spiriferide and spiriferinide brachiopod taxa with a weakly transverse but strongly convex ventral valve are noted to exhibit similar modifications in their spiralia, possibly due to the spatial limitation of their mantle cavities.     

The ideal hydrodynamic form of the concavo‐convex productide brachiopod shell

Shiino, Y & Suzuki, Y. 2011: The ideal hydrodynamic form of the concavo‐convex productide brachiopod shell. Lethaia, Vol. 44, pp. 329–343. Water‐flume experiments were performed to determine whether the concavo‐convex Permian brachiopod Waagenoconcha imperfecta was hydrodynamically adapted for feeding. The generation of passive currents inside the valves was observed experimentally. The use of four transparent, hollow polyhedron models, each differing in a single morphological feature, permitted observation of the currents inside the valves and allowed evaluation of the hydrodynamic significance of the ears and the prominent geniculated trail. Regardless of the direction of ambient flow, only the approximate‐imitation model generated a stable flow pattern consisting of inhalation from the ear gapes and exhalation from the anterior trail gape; models lacking or with small changes in these morphological features failed to generate stable flow patterns. The stable flow pattern was probably maintained by a pressure difference between the posterior lower ear gapes (maximum pressure) and the anterior trail gape (minimum pressure). Notably, bilaterally rotating internal currents formed parallel to the brachial ridges; such flow patterns would facilitate the capture of food particles by the animal via tentacles on its lophophore, which is most likely were located on the brachial ridges. Our results demonstrate that the immobile brachiopod W. imperfecta, an animal incapable of widely opening its valves, probably fed on the passive internal currents generated by its shell form. This unique valve morphology appears to be perfectly adapted from a hydrodynamic point of view. □Biomechanics, ecomorphology, evolution, morphological disparity, Productidina, suspension feeder.     

X-ray computed tomography: A promising tool to investigate the brachiopod shell interior. Effects on 3D modelling and taxonomy

Barremian and Cenomanian rhynchonelliform brachiopods, one Santonian and one Holocene species (Rhynchonellida and Terebratulida), have been observed using X-ray Computed Tomography in order to investigate the shell interior. Compared to transverse serial sections used formerly, X-ray CT is a promising tool. It permits 3D modelling of the brachidium, which is important for brachiopod classification. Four types of brachidium present during the Cretaceous have been observed (crura for the Rhynchonellida, short loop for Terebratulidina–Terebratulidae, ring-loop for Terebratulidina–Cancellothyrididae and long-loop for Terebratellidina), as well as relationships lophophore/brachidium in a Holocene species. Limitations are discussed, including the nature of the sediments enclosed between the valves, diagenesis, and the necessity to observe several age groups concerning the Terebratellidina. Finally, this non-destructive tool facilitates 3D reconstruction of inaccessible brachidia to improve brachiopod taxonomy and as an aid in curating collections.     

Architecture and function of the lophophore in the problematic brachiopod Heliomedusa orienta (Early Cambrian, South China)

The detailed structure of the lophophore is a key diagnostic character in the definition of higher brachiopod taxa. The problematic Heliomedusa orienta Sun and Hou, from the Lower Cambrian Chengjiang Lagerstätte of Yunnan, southwestern China, has a well-preserved lophophore, which is unlike that of any known extant or extinct brachiopods. Based on a comparative study of lophophore disposition in H. orienta and the extant discinid Pelagodiscus atlanticus, the in- and excurrent pattern and shell orientation of H. orienta are described and discussed. Reconstructions of lophophore shape and function are based on numerous specimens and comparison with P. atlanticus. The lophophore is composed of a pair of lophophoral arms that freely arch posteriorly rather than coiling anteriorly as commonly seen in fossil and recent lingulids. The lophophore is attached to the dorsal lobe of the mantle; it has neither calcareous nor chitinous supporting structures, and is disposed symmetrically on either side of the valve midline. The mouth can be inferred to be located at the base of the two brachial tubes, slightly posterior to the anterodorsal projection of the body wall. The lophophoral arms bear laterofrontal tentacles with a double row of cilia along their lateral edge, as in extant lingulid brachiopods. The main brachial axes are also ciliated, which presumably facilitated transport of mucous-bound nutrient particles to the mouth. The unique organization of the lophophore in Heliomedusa is not like any known fossil and living brachiopods. This clearly demonstrates that H. orienta is not a member of any crown group. It is here considered as a member of the brachiopod stem group, which challenges recent interpretations of a close discinid affinity.     

A three‐dimensional geometric morphometric study of the development of sulcus versus shell outline in Permian neospiriferine brachiopods

The morphological variation of the sulcal development and shell outline in large Permian neospiriferine brachiopods including Fasciculatia Waterhouse, 2004 is investigated using geometric morphometrics. The sulcal tongues of spiriferide brachiopods can be, in a qualitative sense, categorized into three types according to the degree of their development: short sulcal tongue, long sulcal tongue and geniculated sulcal tongue. All three types have been noted within Fasciculatia striatoparadoxa, regardless of the nature of the substrate which they originally inhabited. To quantify its morphological variation both in sulcal development and shell outline, 51 brachiopod shells were scanned with a three‐dimensional (3‐D) surface imaging device, and their 3‐D models were reconstructed. Using two landmarks and 58 semilandmarks designated on the surface of the reconstructed 3‐D models, a landmark‐based morphometric analysis was performed. Our result demonstrates a significant intraspecific variation of sulcal development in F. striatoparadoxa and its relatives. Local environmental factors, especially the intensity of ambient water flow, are invoked as the most likely cause for this intraspecific variation. Additionally, this study also shows that there are considerable interspecific distinctions in shell outline among Fasciculatia species, independent of the high variation in the sulcal development. The strong stability of overall shell outline at species level implies a decoupled morphological development between sulcal tongue and whole shell outline. The 3‐D morphometric approach applied here demonstrates its great utility as a tool for quantifying and analysing the morphological variation of highly convex brachiopod shells.     

Particle capture in ciliary filter‐feeding gymnolaemate and phylactolaemate bryozoans – a comparative study

Riisgård, H.U., Okamura, B. and Funch, P. 2009. Particle capture in ciliary filter‐feeding gymnolaemate and phylactolaemate bryozoans – a comparative study. —Acta Zoologica (Stockholm) 91 : 416–425. We studied particle capture using video‐microscopy in two gymnolaemates, the marine cheilostome Electra pilosa and the freshwater ctenostome Paludicella articulata, and three phylactolaemates, Fredericella sultana with a circular funnel‐shaped lophophore, and Cristatella mucedo and Lophophus crystallinus, both with a horseshoe‐shaped lophophore. The video‐microscope observations along with studies of lophophore morphology and ultrastructure indicated that phylactolaemate and gymnolaemate bryozoans with a diversity of lophophore shapes rely on the same basic structures and mechanisms for particle capture. Our study also demonstrates that essential features of the particle capture process resemble one another in bryozoans, brachiopods and phoronids.     

A reconstruction of the lophophore of Devonian rhynchonellids (Brachiopoda) by using X-Ray micro-CT

The X-ray microtomographic study has revealed contrast inclusions (possibly iron compounds) in several shells of Devonian (Emsian–Famennian) rhynchonellids (Brachiopoda) from Transcaucasia. Judging by the location of inclusions, they may correspond to soft tissues of lophophores. The spire-shaped inclusion in the shell of the holotype of the Late Devonian Sharovaella mirabilis Pakhnevich, 2012 has typical features of spirolophe and is interpreted as a part of one of lophophore spires. This find suggests that in the Late Devonian the spirolophe already existed in rhynchonellids. The dorsoventrally directed spirolophous lophophore is an ancient conservative feature of the order Rhynchonellida.     

Morphobiological study of the brachiopods of the order Chonetida

A comparative morphological study of the brachiopods of the order Chonetida revealed a key part of the development of the shell structures connected with the feeding and respiration organs, such as the lophophore, musculature, and mantle, in the morphological evolution of the group. The general trends revealed in the development are adaptive and were restored based on morphofunctional analysis. Against the background of these trends, the correlative changes of the shell shape and its external ornamentation led to the repeated appearance of homeomorphs, whose similarity cannot be explained by adaptation. The phylogeny of the superfamily Anoplioidea is described as an example.     

Paleoecology of Auloporida: an example from the Devonian of the Holy Cross Mts., Poland

Substrate specificity of Auloporida (Tabulata) from the Ska?y Fm. (Upper Eifelian-Lower Givetian) of the Holy Cross Mts., Poland, has been recognized. Kyrtatrypa sp., a rare species in the formation (under 5%), was the most often encrusted brachiopod (59% of investigated specimens), while the most often occurring brachiopod, Aulacella eifeliensis (de Verneuil) was nearly not encrusted. The majority of encrusted brachiopods were larger than 20 mm, while smaller brachiopods occur abundantly in the Formation. The substrate specificity has been caused mainly by the ornamentation of the host's shell. The position of corallites along the commissure of the brachiopod shell proves that auloporids often encrusted living hosts. The epizoan probably used water currents produced by brachiopod's lophophore impoverishing the host's food composition, their relationship can therefore be described as scramble competition.     

Body volumes and internal space constraints in articulate brachiopods

Brachiopods were once dominant in all the oceans of the world. but their distributions are non more restricted. There are few species which are found in shallow warm habitats and these are predominantly small. They have exceptionally low metabolic rates and exhibit low energy lifestyles. The majority of living articulate brachiopods are punctate (possessing mantle extensions. or caeca. which traverse the shell). Evidence produced hei-e suggests that the evolution of these phenomena may have been strongly affected by architectural constraints placed on articulate brachiopods by the use of the lophophore for feeding and respiration. They are essentially space limited because of the large volume needed for this organ. In some punctate brachiopods over 75% of their total body volume may be occupied by the lophophore and mantle cavity. This figure is only 60% in an impunctate (no caeca) species and may be only 20% in bivalve molluses. The implications are that caeca evolved to reduce pressure on space requirements, that maximum sizes may be set by the scaling patterns of space allocation and metabolic efficiency is a consequence of space constraints. Current distribution patterns may be strongly affected by the low metabolism and low energy lifestyles. The relative success of small brachiopods in warm shallow seas may have been facilitated by the scaling patterns of space allocations which show small specimens to have similar mantle cavity volumes to bivalve molluscs.     

The mesolophe, a new lophophore type for chonetacean brachiopods

Rachebaeuf, P. R. & Copper, P. 1990 10 15: The mesolophe, a new lophophore type for chonetacean brachiopods. Lethaia , Val. 23, pp. 341–346. Oslo. ISSN 0024–1164.
Following a summary of previous lophophore reconstructions for the chonetaceans, we describe an unusual pyritized structure within the calcite infill of an exceptionally preserved shell of Archeochonetes primigenius (Twenhofel) from the Late Ordovician (Ashgill) of Anticosti Island, Quebec, Canada. The brachial valve interior of most Lower Devonian to Permian chonetaceans shows the development of three depressed deepened areas (gutters) in the valve floor. The disposition of these gutters coincides remarkably with the shape of the pyritized structure, which we postulate as a new type of lophophore, the mesolophe. ▭ Brachiopoda, Chonetacea, functional morphology, lophophore .     

Determination of paleoseasonality of fossil brachiopods using shell spiral deviations and chemical proxies

Brachiopods have been extensively used in paleoclimatic and paleoecological reconstructions, but their utility would greatly increase if paleoseasonality information could be obtained from their shells. Determining seasonal seawater temperature variations from fossil brachiopods requires knowledge of specimen ontogenetic ages, which is difficult to determine compared to other organisms secreting a shell by accretion. In this study, the combination of the spiral deviation methodology and chemical proxies is tested for determining specimen ontogenetic ages and paleoseasonality using two species of fossil brachiopods, Laqueus rubellus and Terebratula terebratula, of Pleistocene and Late Miocene age, respectively. Spiral deviations were obtained for Laqueus and Terebratula using an R program developed for modern taxa, and well-preserved shells were analyzed using oxygen isotopes and Mg/Ca ratios as chemical proxies for past seawater temperature. Results reveal that locations of spiral deviations on shells of L. rubellus displayed a strong direct relationship with Mg concentrations, and resulting Mg/Ca-derived paleotemperatures were seasonal. Conversely, specimens of T. terebratula did not show a consistently strong relationship between Mg concentrations and spiral deviations, although resulting paleotemperatures agreed with those from previous studies. Overall, the results from this study indicate that the spiral deviation methodology combined with chemical proxies presents great potential for utility in past seasonal seawater temperature reconstructions in pristinely preserved, biconvex fossil brachiopods.     

Modern Data on the Innervation of the Lophophore in Lingula anatina (Brachiopoda) Support the Monophyly of the Lophophorates

Evolutionary relationships among members of the Lophophorata remain unclear. Traditionally, the Lophophorata included three phyla: Brachiopoda, Bryozoa or Ectoprocta, and Phoronida. All species in these phyla have a lophophore, which is regarded as a homologous structure of the lophophorates. Because the organization of the nervous system has been traditionally used to establish relationships among groups of animals, information on the organization of the nervous system in the lophophore of phoronids, brachiopods, and bryozoans may help clarify relationships among the lophophorates. In the current study, the innervation of the lophophore of the inarticulate brachiopod Lingula anatina is investigated by modern methods. The lophophore of L. anatina contains three brachial nerves: the main, accessory, and lower brachial nerves. The main brachial nerve is located at the base of the dorsal side of the brachial fold and gives rise to the cross neurite bundles, which pass through the connective tissue and connect the main and accessory brachial nerves. Nerves emanating from the accessory brachial nerve account for most of the tentacle innervation and comprise the frontal, latero-frontal, and latero-abfrontal neurite bundles. The lower brachial nerve gives rise to the abfrontal neurite bundles of the outer tentacles. Comparative analysis revealed the presence of many similar features in the organization of the lophophore nervous system in phoronids, brachiopods, and bryozoans. The main brachial nerve of L. anatina is similar to the dorsal ganglion of phoronids and the cerebral ganglion of bryozoans. The accessory brachial nerve of L. anatina is similar to the minor nerve ring of phoronids and the circumoral nerve ring of bryozoans. All lophophorates have intertentacular neurite bundles, which innervate adjacent tentacles. The presence of similar nerve elements in the lophophore of phoronids, brachiopods, and bryozoans supports the homology of the lophophore and the monophyly of the lophophorates.