Many animals with external armour, such as hedgehogs, isopods and trilobites, curl into a protect... more Many animals with external armour, such as hedgehogs, isopods and trilobites, curl into a protective ball when disturbed. However, in situations where predators would engulf an exposed animal whole, regardless of position , conglobation may provide limited added defence and the benefits were previously unclear. We show that polyplacophoran molluscs (chitons) are three times less likely to spend time curled into a ball in the presence of a predator. When the cue of a potential predator is present, animals instead spend significantly more time in active, high risk, high reward behaviours such as arching, balancing on the head and tail ends of their girdle and pushing the soft foot up into an exposed position. Arching increases vulnerability , but also can increase the likelihood of rapidly encountering new substratum that would allow the animal to right itself. In some other animals , the ability to roll into a ball is associated with rolling away from danger. Curling into a ball would improve mobility, to be rolled on to a safer position, but reattachment is the higher priority for chitons in the face of danger.
Physiological traits are the foundation of an organism’s success in a dynamic environment, yet ba... more Physiological traits are the foundation of an organism’s success in a dynamic environment, yet basic measurements are unavailable for many taxa and even ecosystems. We measured routine metabolism in two hydrothermal vent gastropods, Alviniconcha marisindica (n = 40) and the scaly-foot gastropod Chrysomallon squamiferum (n = 18), from Kairei and Edmond vent fields on the Central Indian Ridge (23–25°S, about 3000 meter depth). No previous studies have measured metabolism in any Indian Ocean vent animals. After recovering healthy animals to the surface, we performed shipboard closed-chamber respirometry experiments to compare oxygen uptake at different temperatures (10, 16, and 25 °C) at surface pressure (1 atm). The physiology of these species is driven by the demands of their chemoautotrophic symbionts. Chrysomallon has very enlarged respiratory and circulatory systems, and endosymbionts are housed in its trophosome-like internal esophageal gland. By contrast, Alviniconcha has chemoautotrophic bacteria within the gill and less extensive associated anatomical adaptations. Thus, we predicted that routine oxygen consumption of Chrysomallon might be higher than that of Alviniconcha. However, oxygen consumption of Chrysomallon was not higher than that of Alviniconcha, and, further, Chrysomallon maintained a steady metabolic demand in two widely separated experimental temperatures, while Alviniconcha did not. We interpret that these findings indicate that (1) the “trophosome” does not fundamentally increase oxygen requirement compared to other gastropod holobionts, and (2) cold temperatures (10 °C) induce a stress response in Alviniconcha, resulting in aberrantly high uptake. While these two large gastropod species co-occur, differences in oxygen consumption may reflect the separate niches they occupy in the vent ecosystem.
A proposed method to determine chronological age of crustaceans uses putative annual bands in the... more A proposed method to determine chronological age of crustaceans uses putative annual bands in the gastric mill ossicles of the foregut. The interpretation of cuticle bands as growth rings is based on the idea that ossicles are retained through the moult and could accumulate a continuous record of age. However, recent studies presented conflicting findings on the dynamics of gastric mill ossicles during ecdysis. We herein study cuticle bands in ossicles in four species of commercially important decapod crustaceans (Homarus gammarus, Nephrops norvegicus, Cancer pagurus and Necora puber) in different phases of the moult cycle using dissections, light microscopy, micro-computed tomography and cryo-scanning electron microscopy. Our results demonstrate that the gastric mill is moulted and ossicles are not retained but replaced during ecdysis. It is therefore not plausible to conclude that ossicles register a lifetime growth record as annual bands and thereby provide age information. Other mechanisms for the formation of cuticle bands and their correlation to size-based age estimates need to be considered and the effect of moulting on other cuticle structures where 'annual growth bands' have been reported should be investigated urgently. Based on our results, there is no evidence for a causative link between cuticle bands and chronological age, meaning it is unreliable for determining crustacean age.
Life stages of some animals, including amphibians and insects, are so different that they have hi... more Life stages of some animals, including amphibians and insects, are so different that they have historically been seen as different species. ‘Metamorphosis’ broadly encompasses major changes in organism bodies and, importantly, concomitant shifts in trophic strategies. Many marine animals have a biphasic lifestyle, with small pelagic larvae undergoing one or more metamorphic transformations before settling into a permanent, adult morphology on the benthos. Post-settlement, the hydrothermal vent gastropod Gigantopelta chessoia experiences a further, cryptic metamorphosis at body sizes around 5–7 mm. The terminal adult stage is entirely dependent on chemoautotrophic symbionts; smaller individuals do not house symbionts and presumably depend on grazing. Using high-resolution X-ray microtomography to reconstruct the internal organs in a growth series, we show that this sudden transition in small but sexually mature individuals dramatically reconfigures the organs, but is in no way apparent from external morphology. We introduce the term ‘cryptometamorphosis’ to identify this novel phenomenon of a major body change and trophic shift, not related to sexual maturity, transforming only the internal anatomy. Understanding energy flowin ecosystems depends on the feeding ecology of species; the present study highlights the possibility for adult animals to make profound shifts in biology that influence energy dynamics.
The majority of species on Earth are in " under-studied " groups, and indeed probably the majorit... more The majority of species on Earth are in " under-studied " groups, and indeed probably the majority of species remain undiscovered and undescribed. Species are natural units of evolution, and they are formed from branching phylogenetic processes that have a mathematical structure. So it follows that we should be able to develop a set of general principles that describe global patterns of species groups, like genera. Understanding such patterns would lend considerable power to the approach of " taxonomic surrogacy. " In environmental assessments, ecology, and paleontology, it is common to substitute genus-level or family-level identification where definitive species identification is impractical. Clarity and confidence in fundamental patterns, based on a robust null model for species and genus level diversity, can accelerate species discovery: there are more species in the tropics, species-poor genera are very common, large genera are rare. Much hope has been placed in DNA barcoding as an effective tool to increase the pace of species discovery, but it is abundantly clear that certain mitochondrial DNA (mtDNA) markers are more or less variable in different clades and universal threshold values are impractical to delimit species. This study further examines the patterns of divergence in one common mtDNA barcode fragment, cytochrome c oxidase subunit 1 at the genus level. We compared pairwise divergence in this fragment between two animal clades that have similar species richness but different evolutionary histories: birds and bivalves. We analyzed quality controlled alignments of over 39,000 published sequences in 1223 genera. Median pairwise differences at the genus level are positively correlated with the species richness of a genus, and this is not dependent of the number of sequences sampled. Unsurprisingly, sequence divergence in vertebrates was far more constrained than in evolutionarily more ancient non-vertebrate clades. Differences among the groups examined highlight the need for DNA barcode approaches to be considered in the context of specific biological groups. Vertebrates are better studied, but not necessarily representative of the majority of biodiversity. A technique that provides powerful insights for vertebrate species may be ineffective for the majority of organisms.
Molluscs demonstrate astonishing morphological diversity, and the relationships among clades have... more Molluscs demonstrate astonishing morphological diversity, and the relationships among clades have been debated for more than a century. Molluscan nervous systems range from simple 'lad-der-like' cords to the complex brains of cephalopods. Chitons (Polyplacophora) are assumed to retain many molluscan plesiomorphies, lacking neural condensation and ganglionic structure, and therefore a brain. We reconstructed three-dimensional anatomical models of the nervous system in eight species of chitons in an attempt to clarify chiton neuroarchitecture and its variability. We combined new data with digitised historic slide material originally used by malacologist Johannes Thiele (1860–1935). Reconstructions of whole nervous systems in Acanthochitona fascicularis, Callochiton septemvalvis, Chiton olivaceus, Hemiarthrum setulosum, Lepidochitona cinerea, Lepi-dopleurus cajetanus and Leptochiton asellus, and the anterior nervous system of Schizoplax brandtii, demonstrated consistent and substantial anterior neural concentration in the circumoeso-phageal nerve ring. This is further organised into three concentric tracts, corresponding to the lateral, ventral and cerebral nerve cords. These represent homologues to the three main pairs of ganglia in other molluscs. Their relative size, shape and organisation are highly variable among the examined taxa, but consistent with previous studies of select species, and we formulated a set of neuroanatomical characters for chitons. These support anatomical transitions at the ordinal and subordinal levels; the identification of robust homologies in neural architecture will be central to future comparisons across Mollusca and, more broadly, Lophotrochozoa. Contrary to almost all previous descriptions, the size and structure of the chiton anterior nerve ring unambiguously qualify it as a true brain with cordal substructure.
Originally known as fossils from the Cambrian to the Devonian, the finding of a living monoplacop... more Originally known as fossils from the Cambrian to the Devonian, the finding of a living monoplacophoran mollusc in 1952 was one of the great zoological discoveries of the twentieth century. Now, over 35 living species have been documented from deep-sea locations around the world, mainly from samples collected with trawls. Encountering these animals is extremely rare, and in situ observations are scant. Here, we report two new sightings and ecological data for a probable undescribed species of Neopilina including the first ever high-definition close-up video of these monoplacophorans in their natural environment, obtained while exploring seamount environments in American Samoa. Extensive trackways, similar to those associated with the monoplacophoran siting, may be evidence of a larger population at both seamounts. Living monoplacophorans are important to understanding the recent evolution of deep-sea fauna, yet their habitat, on polymetallic nodules and ferromanganese crusts, is under rapidly increasing pressure for deep-sea mineral extraction.
Interactions between Lipophrys pholis and its amphipod prey Echinogammarus marinus were used to i... more Interactions between Lipophrys pholis and its amphipod prey Echinogammarus marinus were used to investigate the effect of changing water temperatures, comparing current and predicted mean summer temperatures. Contrary to expectations, predator attack rates significantly decreased with increasing temperature. Handling times were significantly longer at 19 ∘ C than at 17 and 15 ∘ C and the maximum feeding estimate was significantly lower at 19 ∘ C than at 17 ∘ C. Functional-response type changed from a destabilizing type II to the more stabilizing type III with a temperature increase to 19 ∘ C. This suggests that a temperature increase can mediate refuge for prey at low densities. Predatory pressure by teleosts may be dampened by a large increase in temperature (here from 15 to 19 ∘ C), but a short-term and smaller temperature increase (to 17 ∘ C) may increase destabilizing resource consumption due to high maximum feeding rates; this has implications for the stability of important intertidal ecosystems during warming events.
Allometry involves the study of the relationship between size and shape of an individual, and in ... more Allometry involves the study of the relationship between size and shape of an individual, and in particular, the manner in which shape depends on size. Animals with multi-element skeletons may have differing growth allometries in different parts of the body. Chitons, for example, have eight overlapping shell plates or valves of three distinct types: head (one plate), intermediate (six plates), and tail (one plate). The overall chiton body is ellipsoidal and different species differ in their eccentricity. The aim of this study was to examine overall allometry in size and shape over adult ontogeny, and how these patterns vary among four closely related species of intertidal chitons from Southeastern Pacific Ocean. For each specimen (n = 407), measurements were taken of total body length and the exposed anterio-posterior lengths of the eight shell plates. Multivariate allometry was evaluated by means of a principal component analysis for each species separately, and for the total. The results showed differential allometric growth of specific skeletal elements, which varied among species; however, there was no clear evidence for specific differentiable growth stages. The overall trend among the combined species was for weakly positive allometry of shell plate widths, but isometric growth of total length and width; thus, the lateral proportion of the animal occupied by shell increases over growth and conversely " thinner looking " girdles may be generally indicative of older animals.
A new species of Callochiton, C. stefaniae n. sp., is identified in the framework of investigatio... more A new species of Callochiton, C. stefaniae n. sp., is identified in the framework of investigations aimed to better characterise the Strait of Messina benthic ecosystem. The new species, found in a peculiar facies of hard bottoms densely colonised by the hydrocoral Errina aspera (Linnaeus, 1767), is morphologically distinct from the co-generic Callochiton septemvalvis (Montagu, 1803), living in the Mediterranean Sea and along other European coasts, and C. doriae (Capellini, 1859), living only in the Mediterranean Sea.
Photoreception and vision are fundamental aspects of animal sensory biology and ecology, but impo... more Photoreception and vision are fundamental aspects of animal sensory biology and ecology, but important gaps remain in our understanding of these processes in many species. The colour-changing brittle star Ophiocoma wendtii is iconic in vision research, speculatively possessing a unique whole-body visual system that incorporates information from nerve bundles underlying thousands of crystalline 'microlenses'. The hypothesis that these might form a sophisticated compound eye-like system regulated by chromatophores has been extensively reiterated, with investigations into biomimetic optics and similar supposedly 'visual' structures in living and fossil taxa. However, no photoreceptors or visual behaviours have ever been identified. We present the first evidence of photoreceptor networks in three Ophiocoma species, both with and without microlenses and colour-changing behaviour. High-resolution microscopy, immunohistochemistry and synchrotron tomography demonstrate that putative photoreceptors cover the animals' oral, lateral and aboral surfaces, but are absent at the hypothesized focal points of the microlenses. The structural optics of these crystal 'lenses' are an exaptation and do not fulfil any apparent visual role. This contradicts previous studies, yet the photo-receptor network in Ophiocoma appears even more widespread than previously anticipated, both taxonomically and anatomically.
A genus is a taxonomic unit that may contain one species (monotypic) or thousands. Yet counts of ... more A genus is a taxonomic unit that may contain one species (monotypic) or thousands. Yet counts of genera or families are used to quantify diversity where species-level data are not available. High frequencies of monotypic genera (~30% of animals) have previously been scrutinized as an artefact of human classification. To test whether Linnean taxonomy conflicts with phylogeny, we compared idealized phylogenetic systematics in silico with real-world data. We generated highly replicated, simulated phylogenies under a variety of fixed speciation/extinction rates, imposed three independent taxonomic sorting algorithms on these clades (2.65 × 10 8 simulated species) and compared the resulting genus size data with quality-controlled taxonomy of animal groups (2.8 × 10 5 species). 'Perfect' phylogenetic systematics arrives at similar distributions to real-world taxonomy, regardless of the taxonomic algorithm. Rapid radiations occasionally produce a large genus when speciation rates are favourable; however, small genera can arise in many different ways, from individual lineage persistence and/or extinctions creating subdivisions within a clade. The consistency of this skew distribution in simulation and real-world data, at sufficiently large samples, indicates that specific aspects of its mathematical behaviour could be developed into generalized or nomothetic principles of the global frequency distributions of higher taxa. Importantly, Linnean taxonomy is a better-than-expected reflection of underlying evolutionary patterns.
Seven different ecological feeding strategies have previously been identified among chitons, desp... more Seven different ecological feeding strategies have previously been identified among chitons, despite their apparent morphological homogeneity. These include: detrivores, herbivores, omnivorous grazers, carnivorous grazers, specialist spongivores, epizoophagous feeders, xylophagous wood-dwelling species and true predators. The majority of species among common intertidal chitons appear to be omnivorous grazers. Here, we examined the gut morphology, and radula morphology, in species from various feeding types. The proportionate length and mineralization of the radula are not strongly correlated with feeding type, but these characteristics could be refined and later used to exclude particular habits where no other ecological data are available. Gut length in chitons follows classical gut foreshortening, with ambush predators having a short intestinal tract forming a single major loop, whereas obligate herbivores having dramatically long intestinal lengths with multiple coilings. Multiple feeding strategies, and concomitant adaptation of the digestive system, can be observed among phylogenetically closely-related taxa. Niche partitioning through dietary specialization, even among co-occurring omnivorous grazers, may speculatively underpin the success of chitons in the Northeast Pacific and other regions. How to cite this article: Sigwart J.D., Schwabe E. 2017. Anatomy of the many feeding types in polyplacophoran molluscs // Invert.
One great remaining problem in evolutionary biology is to understand which common ancestor could ... more One great remaining problem in evolutionary biology is to understand which common ancestor could have given rise to descendants as different as giant squid and microscopic pea clams. Two new papers provide important insights into molluscan body plan disparity.
We report observations from a very short survey of micromolluscs collected on the seaweed Caulerp... more We report observations from a very short survey of micromolluscs collected on the seaweed Caulerpa from several sites near Cebu, in the Philippines. We recovered 159 morphospecies of bivalves and gastropods on Caulerpa spp. from point sampling of seaweed from across four markedly different habitats: active aquaculture, disused aquaculture sites, mangrove, and coral rubble.
All scientific and intellectual endeavours advance by building on earlier observations. In organi... more All scientific and intellectual endeavours advance by building on earlier observations. In organismal biology, we can in fact directly replicate original studies of morphology and anatomy, when the original material is still present and accessible in the permanent care of museums. We refer to the apparently miraculous " Lazarisation " of these historical specimens, when the application of state-of-the-art scientific techniques brings new life to material in natural history collections. Classical anatomical, histological and palaeontological work established our fundamental understanding of the natural world over centuries of meticulous and dedicated research, much of which remains unsurpassed to this day. Many of these original specimens are still available to active researchers through dedicated permanent collections in the care of universities and museums. An explosion of advancing methods in recent decades has opened new avenues of research that can exploit invaluable historical material. We review the application of novel techniques, primarily new imaging methods, to historic and important specimens. The pursuit of ultra-high resolution magnification, three-dimensional digital modelling, non-invasive scanning techniques , and, increasingly, elemental analyses all have enormous implications for the future of morphology. Palaeontology, comparative anatomy, and development in particular make ideal platforms for the exploitation of these new techniques. These methods are revolutionizing our use of museum collections and reinventing their role in modern morphological research, which comes at a time of increasing threat to collections and museum curation funding. Future innovations in imaging and non-invasive analyses will doubtless accelerate the renewed research efforts dedicated to existing specimens. Most importantly, we celebrate the continued contributions to morphology from these invaluable pieces of our scientific heritage. How to cite this article: Sumner-Rooney L., Sigwart D. 2017. Lazarus in the museum: resurrecting historic specimens through new technology // Invert.
Up to three miles below the ocean surface, deep-sea hydrothermal vents are home to a community of... more Up to three miles below the ocean surface, deep-sea hydrothermal vents are home to a community of extraordinary mollusks. In an environment without light, under intense pressure and volcanic heat, many gastropods and bivalves living directly on the vent chimneys show adaptations that have driven important scientific breakthroughs. For example, the famous ‘scaly-foot’ gastropod, Chrysomallon squamiferum, has hard scales on its foot with a crystalline iron coating that has inspired novel defensive armor designs. This iconic species has only been reported from three sites in the Indian Ocean, each site hundreds of miles apart and only around half the size of a football field. Two of these three sites are already designated under international exploration licenses for deep-sea mining, to extract rare minerals from the vent chimneys. Economic and political pressures to exploit the seabed are advancing much faster than scientific exploration, putting these vent ecosystems and their molluscan residents at risk.
Things without names are difficult to rationalise, and so species that go without names are diffi... more Things without names are difficult to rationalise, and so species that go without names are difficult to conserve or protect. This is a case study in resolving conflicts in historical taxonomy and 'real' species (identifiable and evo-lutionarily relevant groupings) using an approach including population genetics, natural history, and pragmatism. We report the observation that populations of a shallow-water chiton species from Washington and British Columbia demonstrate extremely high site fidelity and patchy distribution. Their limited dispersal potential and isolation could be explained by a brooding life history. This stands in direct contrast with the supposedly wide distribution of this " species " , Leptochiton rugatus (Carpenter in Pilsbry, 1892) sensu lato, from the Sea of Japan to Baja California. But this lineage has previously been suggested to comprise several cryptic species. Indeed, a haplotype network analysis using 61 individual sequences of the cytochrome oxidase c subunit I gene for L. rugatus s.l. revealed four discrete clusters which correspond to different parts of the geographic range. We infer these to represent four distinct species, at least two of which are likely novel. Leptochiton rugatus sensu stricto is herein reinterpreted as restricted to California and Baja California, and the new name L. cascadiensis sp. nov. is established for the lineage with a distribution in the Cascadia coastal biore-gion from the panhandle of Alaska to Oregon. There are minor morphological differences among these species in the L. rugatus species complex, but genetic data or morphological observations alone would not have been sufficient to definitively recognise these groups as species-level lineages. The observation that different species within the complex may have different life history strategies provides important support for interpreting different populations as genuinely separate species.
Background: Extreme environments prompt the evolution of characteristic adaptations. Yet question... more Background: Extreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Species endemic to deep-sea hydrothermal vents must accommodate high temperature and low pH. The most successful vent species share a constrained pathway to successful energy exploitation: hosting symbionts. The vent-endemic gastropod genus Gigantopelta, from the Southern and Indian Oceans, shares unusual features with a co-occurring peltospirid, the 'scaly-foot gastropod' Chrysomallon squamiferum. Both are unusually large for the clade and share other adaptive features such as a prominent enlarged trophosome-like oesophageal gland, not found in any other vent molluscs. Results: Transmission electron microscopy confirmed endosymbiont bacteria in the oesophageal gland of Gigantopelta, as also seen in Chrysomallon. They are the only known members of their phylum in vent ecosystems hosting internal endosymbionts; other vent molluscs host endosymbionts in or on their gills, or in the mantle cavity. A five-gene phylogenetic reconstruction demonstrated that Gigantopelta and Chrysomallon are not phylogenetically sister-taxa, despite their superficial similarity. Both genera have specialist adaptations to accommodate internalised endosymbionts, but with anatomical differences that indicate separate evolutionary origins. Hosting endosymbionts in an internal organ within the host means that all resources required by the bacteria must be supplied by the animal, rather than directly by the vent fluid. Unlike Chrysomallon, which has an enlarged oesophageal gland throughout post-settlement life, the oesophageal gland in Gigantopelta is proportionally much smaller in juveniles and the animals likely undergo a trophic shift during ontogeny. The circulatory system is hypertrophied in both but the overall size is smaller in Gigantopelta. In contrast with Chrysomallon, Gigantopelta possesses true ganglia and is gonochoristic. Conclusions: Key anatomical differences between Gigantopelta and Chrysomallon demonstrate these two genera acquired a similar way of life through independent and convergent adaptive pathways. What appear to be the holobiont's adaptations to an extreme environment, are driven by optimising bacteria's access to vent nutrients. By comparing Gigantopelta and Chrysomallon, we show that metazoans are capable of rapidly and repeatedly evolving equivalent anatomical adaptations and close-knit relationships with chemoautotrophic bacteria, achieving the same end-product through parallel evolutionary trajectories.
Biogenic habitats, such as coral reefs, facilitate diverse communities. In aquatic systems, aggre... more Biogenic habitats, such as coral reefs, facilitate diverse communities. In aquatic systems, aggregations of mobile benthic species may play a similar ecological role to that of typically sessile biogenic habitats; however, this has rarely been considered. We quantified the abundance of sessile horse mussels Modiolus modiolus and aggregating brittle stars Ophiothrix fragilis and tested for correlations between the density of mussels (live and dead) and brittle stars each with (1) abundance, biomass, diversity, and assemblage structure of associated benthic macrofauna; and (2) percent organic matter of the sediment. We found that the abundance of live M. modiolus was positively associated with the abundance and biomass of macrofauna. The positive association between M. modiolus and macrofaunal abundance was further amplified with an increase in brittle stars and a decrease in dead mussel shells. Macrofaunal biomass was lower with a higher percentage of dead mussel shells, and macrofaunal diversity increased with greater abundances of live M. modiolus and brittle stars. Sediment organic matter was positively related to brittle star density, but not to the abundance of live or dead mussels. The positive relationship between brittlestars and sediment organic matter suggests that brittle stars could enhance rates of benthic−pelagic coupling. Given the importance of understanding the functional role of threatened habitats, it is essential that the underlying community patterns be understood through robust observational studies to then derive testable hypotheses to determine drivers. These findings provide novel insight into the ecological role of aggregations of mobile species, which is essential to prioritize conservation and restoration strategies.
Many animals with external armour, such as hedgehogs, isopods and trilobites, curl into a protect... more Many animals with external armour, such as hedgehogs, isopods and trilobites, curl into a protective ball when disturbed. However, in situations where predators would engulf an exposed animal whole, regardless of position , conglobation may provide limited added defence and the benefits were previously unclear. We show that polyplacophoran molluscs (chitons) are three times less likely to spend time curled into a ball in the presence of a predator. When the cue of a potential predator is present, animals instead spend significantly more time in active, high risk, high reward behaviours such as arching, balancing on the head and tail ends of their girdle and pushing the soft foot up into an exposed position. Arching increases vulnerability , but also can increase the likelihood of rapidly encountering new substratum that would allow the animal to right itself. In some other animals , the ability to roll into a ball is associated with rolling away from danger. Curling into a ball would improve mobility, to be rolled on to a safer position, but reattachment is the higher priority for chitons in the face of danger.
Physiological traits are the foundation of an organism’s success in a dynamic environment, yet ba... more Physiological traits are the foundation of an organism’s success in a dynamic environment, yet basic measurements are unavailable for many taxa and even ecosystems. We measured routine metabolism in two hydrothermal vent gastropods, Alviniconcha marisindica (n = 40) and the scaly-foot gastropod Chrysomallon squamiferum (n = 18), from Kairei and Edmond vent fields on the Central Indian Ridge (23–25°S, about 3000 meter depth). No previous studies have measured metabolism in any Indian Ocean vent animals. After recovering healthy animals to the surface, we performed shipboard closed-chamber respirometry experiments to compare oxygen uptake at different temperatures (10, 16, and 25 °C) at surface pressure (1 atm). The physiology of these species is driven by the demands of their chemoautotrophic symbionts. Chrysomallon has very enlarged respiratory and circulatory systems, and endosymbionts are housed in its trophosome-like internal esophageal gland. By contrast, Alviniconcha has chemoautotrophic bacteria within the gill and less extensive associated anatomical adaptations. Thus, we predicted that routine oxygen consumption of Chrysomallon might be higher than that of Alviniconcha. However, oxygen consumption of Chrysomallon was not higher than that of Alviniconcha, and, further, Chrysomallon maintained a steady metabolic demand in two widely separated experimental temperatures, while Alviniconcha did not. We interpret that these findings indicate that (1) the “trophosome” does not fundamentally increase oxygen requirement compared to other gastropod holobionts, and (2) cold temperatures (10 °C) induce a stress response in Alviniconcha, resulting in aberrantly high uptake. While these two large gastropod species co-occur, differences in oxygen consumption may reflect the separate niches they occupy in the vent ecosystem.
A proposed method to determine chronological age of crustaceans uses putative annual bands in the... more A proposed method to determine chronological age of crustaceans uses putative annual bands in the gastric mill ossicles of the foregut. The interpretation of cuticle bands as growth rings is based on the idea that ossicles are retained through the moult and could accumulate a continuous record of age. However, recent studies presented conflicting findings on the dynamics of gastric mill ossicles during ecdysis. We herein study cuticle bands in ossicles in four species of commercially important decapod crustaceans (Homarus gammarus, Nephrops norvegicus, Cancer pagurus and Necora puber) in different phases of the moult cycle using dissections, light microscopy, micro-computed tomography and cryo-scanning electron microscopy. Our results demonstrate that the gastric mill is moulted and ossicles are not retained but replaced during ecdysis. It is therefore not plausible to conclude that ossicles register a lifetime growth record as annual bands and thereby provide age information. Other mechanisms for the formation of cuticle bands and their correlation to size-based age estimates need to be considered and the effect of moulting on other cuticle structures where 'annual growth bands' have been reported should be investigated urgently. Based on our results, there is no evidence for a causative link between cuticle bands and chronological age, meaning it is unreliable for determining crustacean age.
Life stages of some animals, including amphibians and insects, are so different that they have hi... more Life stages of some animals, including amphibians and insects, are so different that they have historically been seen as different species. ‘Metamorphosis’ broadly encompasses major changes in organism bodies and, importantly, concomitant shifts in trophic strategies. Many marine animals have a biphasic lifestyle, with small pelagic larvae undergoing one or more metamorphic transformations before settling into a permanent, adult morphology on the benthos. Post-settlement, the hydrothermal vent gastropod Gigantopelta chessoia experiences a further, cryptic metamorphosis at body sizes around 5–7 mm. The terminal adult stage is entirely dependent on chemoautotrophic symbionts; smaller individuals do not house symbionts and presumably depend on grazing. Using high-resolution X-ray microtomography to reconstruct the internal organs in a growth series, we show that this sudden transition in small but sexually mature individuals dramatically reconfigures the organs, but is in no way apparent from external morphology. We introduce the term ‘cryptometamorphosis’ to identify this novel phenomenon of a major body change and trophic shift, not related to sexual maturity, transforming only the internal anatomy. Understanding energy flowin ecosystems depends on the feeding ecology of species; the present study highlights the possibility for adult animals to make profound shifts in biology that influence energy dynamics.
The majority of species on Earth are in " under-studied " groups, and indeed probably the majorit... more The majority of species on Earth are in " under-studied " groups, and indeed probably the majority of species remain undiscovered and undescribed. Species are natural units of evolution, and they are formed from branching phylogenetic processes that have a mathematical structure. So it follows that we should be able to develop a set of general principles that describe global patterns of species groups, like genera. Understanding such patterns would lend considerable power to the approach of " taxonomic surrogacy. " In environmental assessments, ecology, and paleontology, it is common to substitute genus-level or family-level identification where definitive species identification is impractical. Clarity and confidence in fundamental patterns, based on a robust null model for species and genus level diversity, can accelerate species discovery: there are more species in the tropics, species-poor genera are very common, large genera are rare. Much hope has been placed in DNA barcoding as an effective tool to increase the pace of species discovery, but it is abundantly clear that certain mitochondrial DNA (mtDNA) markers are more or less variable in different clades and universal threshold values are impractical to delimit species. This study further examines the patterns of divergence in one common mtDNA barcode fragment, cytochrome c oxidase subunit 1 at the genus level. We compared pairwise divergence in this fragment between two animal clades that have similar species richness but different evolutionary histories: birds and bivalves. We analyzed quality controlled alignments of over 39,000 published sequences in 1223 genera. Median pairwise differences at the genus level are positively correlated with the species richness of a genus, and this is not dependent of the number of sequences sampled. Unsurprisingly, sequence divergence in vertebrates was far more constrained than in evolutionarily more ancient non-vertebrate clades. Differences among the groups examined highlight the need for DNA barcode approaches to be considered in the context of specific biological groups. Vertebrates are better studied, but not necessarily representative of the majority of biodiversity. A technique that provides powerful insights for vertebrate species may be ineffective for the majority of organisms.
Molluscs demonstrate astonishing morphological diversity, and the relationships among clades have... more Molluscs demonstrate astonishing morphological diversity, and the relationships among clades have been debated for more than a century. Molluscan nervous systems range from simple 'lad-der-like' cords to the complex brains of cephalopods. Chitons (Polyplacophora) are assumed to retain many molluscan plesiomorphies, lacking neural condensation and ganglionic structure, and therefore a brain. We reconstructed three-dimensional anatomical models of the nervous system in eight species of chitons in an attempt to clarify chiton neuroarchitecture and its variability. We combined new data with digitised historic slide material originally used by malacologist Johannes Thiele (1860–1935). Reconstructions of whole nervous systems in Acanthochitona fascicularis, Callochiton septemvalvis, Chiton olivaceus, Hemiarthrum setulosum, Lepidochitona cinerea, Lepi-dopleurus cajetanus and Leptochiton asellus, and the anterior nervous system of Schizoplax brandtii, demonstrated consistent and substantial anterior neural concentration in the circumoeso-phageal nerve ring. This is further organised into three concentric tracts, corresponding to the lateral, ventral and cerebral nerve cords. These represent homologues to the three main pairs of ganglia in other molluscs. Their relative size, shape and organisation are highly variable among the examined taxa, but consistent with previous studies of select species, and we formulated a set of neuroanatomical characters for chitons. These support anatomical transitions at the ordinal and subordinal levels; the identification of robust homologies in neural architecture will be central to future comparisons across Mollusca and, more broadly, Lophotrochozoa. Contrary to almost all previous descriptions, the size and structure of the chiton anterior nerve ring unambiguously qualify it as a true brain with cordal substructure.
Originally known as fossils from the Cambrian to the Devonian, the finding of a living monoplacop... more Originally known as fossils from the Cambrian to the Devonian, the finding of a living monoplacophoran mollusc in 1952 was one of the great zoological discoveries of the twentieth century. Now, over 35 living species have been documented from deep-sea locations around the world, mainly from samples collected with trawls. Encountering these animals is extremely rare, and in situ observations are scant. Here, we report two new sightings and ecological data for a probable undescribed species of Neopilina including the first ever high-definition close-up video of these monoplacophorans in their natural environment, obtained while exploring seamount environments in American Samoa. Extensive trackways, similar to those associated with the monoplacophoran siting, may be evidence of a larger population at both seamounts. Living monoplacophorans are important to understanding the recent evolution of deep-sea fauna, yet their habitat, on polymetallic nodules and ferromanganese crusts, is under rapidly increasing pressure for deep-sea mineral extraction.
Interactions between Lipophrys pholis and its amphipod prey Echinogammarus marinus were used to i... more Interactions between Lipophrys pholis and its amphipod prey Echinogammarus marinus were used to investigate the effect of changing water temperatures, comparing current and predicted mean summer temperatures. Contrary to expectations, predator attack rates significantly decreased with increasing temperature. Handling times were significantly longer at 19 ∘ C than at 17 and 15 ∘ C and the maximum feeding estimate was significantly lower at 19 ∘ C than at 17 ∘ C. Functional-response type changed from a destabilizing type II to the more stabilizing type III with a temperature increase to 19 ∘ C. This suggests that a temperature increase can mediate refuge for prey at low densities. Predatory pressure by teleosts may be dampened by a large increase in temperature (here from 15 to 19 ∘ C), but a short-term and smaller temperature increase (to 17 ∘ C) may increase destabilizing resource consumption due to high maximum feeding rates; this has implications for the stability of important intertidal ecosystems during warming events.
Allometry involves the study of the relationship between size and shape of an individual, and in ... more Allometry involves the study of the relationship between size and shape of an individual, and in particular, the manner in which shape depends on size. Animals with multi-element skeletons may have differing growth allometries in different parts of the body. Chitons, for example, have eight overlapping shell plates or valves of three distinct types: head (one plate), intermediate (six plates), and tail (one plate). The overall chiton body is ellipsoidal and different species differ in their eccentricity. The aim of this study was to examine overall allometry in size and shape over adult ontogeny, and how these patterns vary among four closely related species of intertidal chitons from Southeastern Pacific Ocean. For each specimen (n = 407), measurements were taken of total body length and the exposed anterio-posterior lengths of the eight shell plates. Multivariate allometry was evaluated by means of a principal component analysis for each species separately, and for the total. The results showed differential allometric growth of specific skeletal elements, which varied among species; however, there was no clear evidence for specific differentiable growth stages. The overall trend among the combined species was for weakly positive allometry of shell plate widths, but isometric growth of total length and width; thus, the lateral proportion of the animal occupied by shell increases over growth and conversely " thinner looking " girdles may be generally indicative of older animals.
A new species of Callochiton, C. stefaniae n. sp., is identified in the framework of investigatio... more A new species of Callochiton, C. stefaniae n. sp., is identified in the framework of investigations aimed to better characterise the Strait of Messina benthic ecosystem. The new species, found in a peculiar facies of hard bottoms densely colonised by the hydrocoral Errina aspera (Linnaeus, 1767), is morphologically distinct from the co-generic Callochiton septemvalvis (Montagu, 1803), living in the Mediterranean Sea and along other European coasts, and C. doriae (Capellini, 1859), living only in the Mediterranean Sea.
Photoreception and vision are fundamental aspects of animal sensory biology and ecology, but impo... more Photoreception and vision are fundamental aspects of animal sensory biology and ecology, but important gaps remain in our understanding of these processes in many species. The colour-changing brittle star Ophiocoma wendtii is iconic in vision research, speculatively possessing a unique whole-body visual system that incorporates information from nerve bundles underlying thousands of crystalline 'microlenses'. The hypothesis that these might form a sophisticated compound eye-like system regulated by chromatophores has been extensively reiterated, with investigations into biomimetic optics and similar supposedly 'visual' structures in living and fossil taxa. However, no photoreceptors or visual behaviours have ever been identified. We present the first evidence of photoreceptor networks in three Ophiocoma species, both with and without microlenses and colour-changing behaviour. High-resolution microscopy, immunohistochemistry and synchrotron tomography demonstrate that putative photoreceptors cover the animals' oral, lateral and aboral surfaces, but are absent at the hypothesized focal points of the microlenses. The structural optics of these crystal 'lenses' are an exaptation and do not fulfil any apparent visual role. This contradicts previous studies, yet the photo-receptor network in Ophiocoma appears even more widespread than previously anticipated, both taxonomically and anatomically.
A genus is a taxonomic unit that may contain one species (monotypic) or thousands. Yet counts of ... more A genus is a taxonomic unit that may contain one species (monotypic) or thousands. Yet counts of genera or families are used to quantify diversity where species-level data are not available. High frequencies of monotypic genera (~30% of animals) have previously been scrutinized as an artefact of human classification. To test whether Linnean taxonomy conflicts with phylogeny, we compared idealized phylogenetic systematics in silico with real-world data. We generated highly replicated, simulated phylogenies under a variety of fixed speciation/extinction rates, imposed three independent taxonomic sorting algorithms on these clades (2.65 × 10 8 simulated species) and compared the resulting genus size data with quality-controlled taxonomy of animal groups (2.8 × 10 5 species). 'Perfect' phylogenetic systematics arrives at similar distributions to real-world taxonomy, regardless of the taxonomic algorithm. Rapid radiations occasionally produce a large genus when speciation rates are favourable; however, small genera can arise in many different ways, from individual lineage persistence and/or extinctions creating subdivisions within a clade. The consistency of this skew distribution in simulation and real-world data, at sufficiently large samples, indicates that specific aspects of its mathematical behaviour could be developed into generalized or nomothetic principles of the global frequency distributions of higher taxa. Importantly, Linnean taxonomy is a better-than-expected reflection of underlying evolutionary patterns.
Seven different ecological feeding strategies have previously been identified among chitons, desp... more Seven different ecological feeding strategies have previously been identified among chitons, despite their apparent morphological homogeneity. These include: detrivores, herbivores, omnivorous grazers, carnivorous grazers, specialist spongivores, epizoophagous feeders, xylophagous wood-dwelling species and true predators. The majority of species among common intertidal chitons appear to be omnivorous grazers. Here, we examined the gut morphology, and radula morphology, in species from various feeding types. The proportionate length and mineralization of the radula are not strongly correlated with feeding type, but these characteristics could be refined and later used to exclude particular habits where no other ecological data are available. Gut length in chitons follows classical gut foreshortening, with ambush predators having a short intestinal tract forming a single major loop, whereas obligate herbivores having dramatically long intestinal lengths with multiple coilings. Multiple feeding strategies, and concomitant adaptation of the digestive system, can be observed among phylogenetically closely-related taxa. Niche partitioning through dietary specialization, even among co-occurring omnivorous grazers, may speculatively underpin the success of chitons in the Northeast Pacific and other regions. How to cite this article: Sigwart J.D., Schwabe E. 2017. Anatomy of the many feeding types in polyplacophoran molluscs // Invert.
One great remaining problem in evolutionary biology is to understand which common ancestor could ... more One great remaining problem in evolutionary biology is to understand which common ancestor could have given rise to descendants as different as giant squid and microscopic pea clams. Two new papers provide important insights into molluscan body plan disparity.
We report observations from a very short survey of micromolluscs collected on the seaweed Caulerp... more We report observations from a very short survey of micromolluscs collected on the seaweed Caulerpa from several sites near Cebu, in the Philippines. We recovered 159 morphospecies of bivalves and gastropods on Caulerpa spp. from point sampling of seaweed from across four markedly different habitats: active aquaculture, disused aquaculture sites, mangrove, and coral rubble.
All scientific and intellectual endeavours advance by building on earlier observations. In organi... more All scientific and intellectual endeavours advance by building on earlier observations. In organismal biology, we can in fact directly replicate original studies of morphology and anatomy, when the original material is still present and accessible in the permanent care of museums. We refer to the apparently miraculous " Lazarisation " of these historical specimens, when the application of state-of-the-art scientific techniques brings new life to material in natural history collections. Classical anatomical, histological and palaeontological work established our fundamental understanding of the natural world over centuries of meticulous and dedicated research, much of which remains unsurpassed to this day. Many of these original specimens are still available to active researchers through dedicated permanent collections in the care of universities and museums. An explosion of advancing methods in recent decades has opened new avenues of research that can exploit invaluable historical material. We review the application of novel techniques, primarily new imaging methods, to historic and important specimens. The pursuit of ultra-high resolution magnification, three-dimensional digital modelling, non-invasive scanning techniques , and, increasingly, elemental analyses all have enormous implications for the future of morphology. Palaeontology, comparative anatomy, and development in particular make ideal platforms for the exploitation of these new techniques. These methods are revolutionizing our use of museum collections and reinventing their role in modern morphological research, which comes at a time of increasing threat to collections and museum curation funding. Future innovations in imaging and non-invasive analyses will doubtless accelerate the renewed research efforts dedicated to existing specimens. Most importantly, we celebrate the continued contributions to morphology from these invaluable pieces of our scientific heritage. How to cite this article: Sumner-Rooney L., Sigwart D. 2017. Lazarus in the museum: resurrecting historic specimens through new technology // Invert.
Up to three miles below the ocean surface, deep-sea hydrothermal vents are home to a community of... more Up to three miles below the ocean surface, deep-sea hydrothermal vents are home to a community of extraordinary mollusks. In an environment without light, under intense pressure and volcanic heat, many gastropods and bivalves living directly on the vent chimneys show adaptations that have driven important scientific breakthroughs. For example, the famous ‘scaly-foot’ gastropod, Chrysomallon squamiferum, has hard scales on its foot with a crystalline iron coating that has inspired novel defensive armor designs. This iconic species has only been reported from three sites in the Indian Ocean, each site hundreds of miles apart and only around half the size of a football field. Two of these three sites are already designated under international exploration licenses for deep-sea mining, to extract rare minerals from the vent chimneys. Economic and political pressures to exploit the seabed are advancing much faster than scientific exploration, putting these vent ecosystems and their molluscan residents at risk.
Things without names are difficult to rationalise, and so species that go without names are diffi... more Things without names are difficult to rationalise, and so species that go without names are difficult to conserve or protect. This is a case study in resolving conflicts in historical taxonomy and 'real' species (identifiable and evo-lutionarily relevant groupings) using an approach including population genetics, natural history, and pragmatism. We report the observation that populations of a shallow-water chiton species from Washington and British Columbia demonstrate extremely high site fidelity and patchy distribution. Their limited dispersal potential and isolation could be explained by a brooding life history. This stands in direct contrast with the supposedly wide distribution of this " species " , Leptochiton rugatus (Carpenter in Pilsbry, 1892) sensu lato, from the Sea of Japan to Baja California. But this lineage has previously been suggested to comprise several cryptic species. Indeed, a haplotype network analysis using 61 individual sequences of the cytochrome oxidase c subunit I gene for L. rugatus s.l. revealed four discrete clusters which correspond to different parts of the geographic range. We infer these to represent four distinct species, at least two of which are likely novel. Leptochiton rugatus sensu stricto is herein reinterpreted as restricted to California and Baja California, and the new name L. cascadiensis sp. nov. is established for the lineage with a distribution in the Cascadia coastal biore-gion from the panhandle of Alaska to Oregon. There are minor morphological differences among these species in the L. rugatus species complex, but genetic data or morphological observations alone would not have been sufficient to definitively recognise these groups as species-level lineages. The observation that different species within the complex may have different life history strategies provides important support for interpreting different populations as genuinely separate species.
Background: Extreme environments prompt the evolution of characteristic adaptations. Yet question... more Background: Extreme environments prompt the evolution of characteristic adaptations. Yet questions remain about whether radiations in extreme environments originate from a single lineage that masters a key adaptive pathway, or if the same features can arise in parallel through convergence. Species endemic to deep-sea hydrothermal vents must accommodate high temperature and low pH. The most successful vent species share a constrained pathway to successful energy exploitation: hosting symbionts. The vent-endemic gastropod genus Gigantopelta, from the Southern and Indian Oceans, shares unusual features with a co-occurring peltospirid, the 'scaly-foot gastropod' Chrysomallon squamiferum. Both are unusually large for the clade and share other adaptive features such as a prominent enlarged trophosome-like oesophageal gland, not found in any other vent molluscs. Results: Transmission electron microscopy confirmed endosymbiont bacteria in the oesophageal gland of Gigantopelta, as also seen in Chrysomallon. They are the only known members of their phylum in vent ecosystems hosting internal endosymbionts; other vent molluscs host endosymbionts in or on their gills, or in the mantle cavity. A five-gene phylogenetic reconstruction demonstrated that Gigantopelta and Chrysomallon are not phylogenetically sister-taxa, despite their superficial similarity. Both genera have specialist adaptations to accommodate internalised endosymbionts, but with anatomical differences that indicate separate evolutionary origins. Hosting endosymbionts in an internal organ within the host means that all resources required by the bacteria must be supplied by the animal, rather than directly by the vent fluid. Unlike Chrysomallon, which has an enlarged oesophageal gland throughout post-settlement life, the oesophageal gland in Gigantopelta is proportionally much smaller in juveniles and the animals likely undergo a trophic shift during ontogeny. The circulatory system is hypertrophied in both but the overall size is smaller in Gigantopelta. In contrast with Chrysomallon, Gigantopelta possesses true ganglia and is gonochoristic. Conclusions: Key anatomical differences between Gigantopelta and Chrysomallon demonstrate these two genera acquired a similar way of life through independent and convergent adaptive pathways. What appear to be the holobiont's adaptations to an extreme environment, are driven by optimising bacteria's access to vent nutrients. By comparing Gigantopelta and Chrysomallon, we show that metazoans are capable of rapidly and repeatedly evolving equivalent anatomical adaptations and close-knit relationships with chemoautotrophic bacteria, achieving the same end-product through parallel evolutionary trajectories.
Biogenic habitats, such as coral reefs, facilitate diverse communities. In aquatic systems, aggre... more Biogenic habitats, such as coral reefs, facilitate diverse communities. In aquatic systems, aggregations of mobile benthic species may play a similar ecological role to that of typically sessile biogenic habitats; however, this has rarely been considered. We quantified the abundance of sessile horse mussels Modiolus modiolus and aggregating brittle stars Ophiothrix fragilis and tested for correlations between the density of mussels (live and dead) and brittle stars each with (1) abundance, biomass, diversity, and assemblage structure of associated benthic macrofauna; and (2) percent organic matter of the sediment. We found that the abundance of live M. modiolus was positively associated with the abundance and biomass of macrofauna. The positive association between M. modiolus and macrofaunal abundance was further amplified with an increase in brittle stars and a decrease in dead mussel shells. Macrofaunal biomass was lower with a higher percentage of dead mussel shells, and macrofaunal diversity increased with greater abundances of live M. modiolus and brittle stars. Sediment organic matter was positively related to brittle star density, but not to the abundance of live or dead mussels. The positive relationship between brittlestars and sediment organic matter suggests that brittle stars could enhance rates of benthic−pelagic coupling. Given the importance of understanding the functional role of threatened habitats, it is essential that the underlying community patterns be understood through robust observational studies to then derive testable hypotheses to determine drivers. These findings provide novel insight into the ecological role of aggregations of mobile species, which is essential to prioritize conservation and restoration strategies.
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