Biological BulletinPub Date : 2023-04-01Epub Date: 2023-08-16DOI: 10.1086/726774
Nicholas D Holland, Linda Z Holland
{"title":"Cephalochordate Hemocytes: First Demonstration for <i>Asymmetron lucayanum</i> (Bahamas Lancelet) Plus Augmented Description for <i>Branchiostoma floridae</i> (Florida Amphioxus).","authors":"Nicholas D Holland, Linda Z Holland","doi":"10.1086/726774","DOIUrl":"10.1086/726774","url":null,"abstract":"<p><p>AbstractWithin phylum Chordata, the subphylum Cephalochordata (amphioxus and lancelets) has figured large in considerations of the evolutionary origin of the vertebrates. To date, these discussions have been predominantly based on knowledge of a single cephalochordate genus (<i>Branchiostoma</i>), almost to the exclusion of the other two genera (<i>Asymmetron</i> and <i>Epigonichthys</i>). This uneven pattern is illustrated by cephalochordate hematology, until now known entirely from work done on <i>Branchiostoma</i>. The main part of the present study is to describe hemocytes in the dorsal aorta of a species of <i>Asymmetron</i> by serial block-face scanning electron microscopy. This technique, which demonstrates three-dimensional fine structure, showed that the hemocytes have a relatively uniform morphology characterized by an oval shape and scanty cytoplasm. Ancillary information is also included for <i>Branchiostoma</i> hemocytes, known from previous studies to have relatively abundant cytoplasm; our serial block-face scanning electron microscopy provides more comprehensive views of the highly variable shapes of these cells, which typically extend one or several pseudopodium-like protrusions. The marked difference in hemocyte morphology found between <i>Asymmetron</i> and <i>Branchiostoma</i> was unexpected and directs attention to investigating comparable cells in the genus <i>Epigonichthys</i>. A broader knowledge of the hemocytes in all three cephalochordate genera would provide more balanced insights into the evolution of vertebrate hematopoiesis.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 2","pages":"71-81"},"PeriodicalIF":1.6,"publicationDate":"2023-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41174639","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Biological BulletinPub Date : 2023-04-01Epub Date: 2023-08-31DOI: 10.1086/726773
Peter K D Hovland, Jose A Tochihuitl, John T Birmingham
{"title":"A Feeding-Related Mechanoreceptor Identified in the Crab <i>Cancer borealis</i> Shares Similarities and Differences with Homologs in Other Crustaceans.","authors":"Peter K D Hovland, Jose A Tochihuitl, John T Birmingham","doi":"10.1086/726773","DOIUrl":"10.1086/726773","url":null,"abstract":"<p><p>AbstractSensory feedback plays an essential role in shaping rhythmic animal movements. In the crustacean stomatogastric nervous system, which is responsible for grinding and filtering food particles in the animal's foregut, a number of mechanoreceptors whose activity affects motor output have been characterized. The hepatopancreas duct receptor neurons, which are located in the pyloric region of the foregut that is responsible for filtering, are among the less well understood groups of stomatogastric mechanoreceptors. Although they were first described decades ago in a number of decapod species, many questions remain about their role in shaping the movements produced by the stomatogastric nervous system. Here we provide the first anatomical and physiological evidence that there are also hepatopancreas duct receptors in the crab <i>Cancer borealis</i>, and we demonstrate that hepatopancreas duct receptor spiking produced by mechanical stimulation modifies the properties of an ongoing pyloric motor program.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 2","pages":"128-137"},"PeriodicalIF":1.6,"publicationDate":"2023-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41177501","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Biological BulletinPub Date : 2023-04-01Epub Date: 2023-08-18DOI: 10.1086/726772
Ryosuke Kimbara, Hisanori Kohtsuka, Toru Miura
{"title":"Differences of Sucker Formation Processes Depending on Benthic or Pelagic Posthatching Lifestyles in Two Octopus Species.","authors":"Ryosuke Kimbara, Hisanori Kohtsuka, Toru Miura","doi":"10.1086/726772","DOIUrl":"10.1086/726772","url":null,"abstract":"<p><p>AbstractMorphologies of animal appendages are highly diversified depending on animal lifestyles. In cephalopods (Mollusca, Cephalopoda), an individual possesses multiple arms that contribute to elaborate behaviors, and suckers on them enable various arm functions. In octopus hatchlings, arm and sucker morphologies can be divided into two different types due to alternative posthatching lifestyles, that is, pelagic or benthic lifestyles, although the underlying developmental differences have yet to be elucidated. In this study, therefore, detailed developmental processes of arms and suckers were observed during embryogenesis in two different octopus species, <i>Octopus parvus</i> and <i>Amphioctopus fangsiao</i>, showing pelagic and benthic posthatching lifestyles, respectively. In <i>O. parvus</i>, sucker formation stopped at a relatively early stage in which three suckers on an arm were produced. In addition, at late embryonic stages, cell proliferation was hardly detected in whole arms, while in <i>A. fangsiao</i>, sucker production continued throughout embryogenesis and cell proliferation also remained active in whole arms even in the late stages. Therefore, although further investigations in other octopus species are required, it is suggested that in octopus evolution, the developmental program of suckers has been modified in accordance with the acquisition of a novel lifestyle.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 2","pages":"82-93"},"PeriodicalIF":1.6,"publicationDate":"2023-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41158560","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Biological BulletinPub Date : 2023-04-01Epub Date: 2023-07-26DOI: 10.1086/725633
Danielle K Barnes, Jonathan D Allen
{"title":"Predators Induce Phenotypic Plasticity in Echinoderms across Life History Stages.","authors":"Danielle K Barnes, Jonathan D Allen","doi":"10.1086/725633","DOIUrl":"10.1086/725633","url":null,"abstract":"<p><p>AbstractMarine invertebrates with biphasic life cycles feature life history transitions that coincide with habitat changes from benthic adults to planktonic embryos and larvae, then a return to the benthos as a juvenile at metamorphosis. The metamorphic transition exposes animals to a new suite of benthic predators, and high mortality often occurs in the hours and days following settlement. Juvenile invertebrates may produce phenotypically plastic morphological defenses when predator cues are detected. However, time lags inherent to phenotypic plasticity may delay the production of defenses until after the period of highest vulnerability. It should, therefore, be beneficial for planktonic larvae approaching settlement to detect waterborne cues from benthic predators and produce juvenile phenotypes appropriate for postmetamorphic survival. Echinoderms are useful models for testing transhabitat and trans-life history stage phenotypic plasticity because many species have larvae that construct their juvenile phenotype while still in the water column. In this study, we tested whether planktonic echinoderm larvae exposed to cues from benthic predators modified their juvenile phenotypes at settlement. Green urchin (<i>Strongylocentrotus droebachiensis</i>) and Pacific sand dollar (<i>Dendraster excentricus</i>) larvae were exposed to predatory green crab (<i>Carcinus maenus</i>) or red rock crab (<i>Cancer productus</i>) cues, respectively, from their early-stage juvenile rudiment formation through settlement. Green urchin larvae exposed to predator cues settled with significantly more juvenile spines compared to unexposed controls. Sand dollars exhibited earlier settlement, larger disk area, fewer spines, and shorter spines when exposed to benthic predator cues. Sand dollar larvae were also exposed to cues from planktonic crab larvae and in response settled sooner and larger, with even fewer and shorter spines than those exposed to benthic predator cues. These results suggest that echinoderm larvae alter their juvenile phenotype in response to predator cues, but the response varies between species, and responses to planktonic threats may be prioritized over benthic ones.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 2","pages":"103-114"},"PeriodicalIF":1.6,"publicationDate":"2023-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41160267","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Biological BulletinPub Date : 2023-04-01Epub Date: 2023-08-04DOI: 10.1086/725689
Veronica Rivi, Anuradha Batabyal, Cristina Benatti, Fabio Tascedda, Joan M C Blom, Ken Lukowiak
{"title":"A Novel Behavioral Display in <i>Lymnaea</i> Induced by Quercetin and Hypoxia.","authors":"Veronica Rivi, Anuradha Batabyal, Cristina Benatti, Fabio Tascedda, Joan M C Blom, Ken Lukowiak","doi":"10.1086/725689","DOIUrl":"10.1086/725689","url":null,"abstract":"<p><p>AbstractThe pond snail <i>Lymnaea stagnalis</i> employs aerial respiration under hypoxia and can be operantly conditioned to reduce this behavior. When applied individually, a heat shock (30 °C for 1 h) and the flavonoid quercetin enhance long-term memory formation for the operant conditioning of aerial respiration. However, when snails are exposed to quercetin before the heat shock, long-term memory is no longer enhanced. This is because quercetin prevents the heat-induced upregulation of heat-shock proteins 70 and 40. When we tested the memory outcome of operant conditioning due to the simultaneous exposure to quercetin and 30 °C, we found that <i>Lymnaea</i> entered a quiescent survival state. The same behavioral response occurred when snails were simultaneously exposed to quercetin and pond water made hypoxic by bubbling nitrogen through it. Thus, in this study, we performed six experiments to propose a physiological explanation for that curious behavioral response. Our results suggest that bubbling nitrogen in pond water, heating pond water to 30 °C, and bubbling nitrogen in 30 °C pond water create a hypoxic environment, to which organisms may respond by upregulating the heat-shock protein system. On the other hand, when snails experience quercetin together with these hypoxic conditions, they can no longer express the physiological stress response evoked by heat or hypoxia. Thus, the quiescent survival state could be an emergency response to survive the hypoxic condition when the heat-shock proteins cannot be activated.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 2","pages":"115-127"},"PeriodicalIF":1.6,"publicationDate":"2023-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"41172706","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Locomotory Palp Function in Interstitial Annelids.","authors":"Will M Ballentine, Kelly M Dorgan","doi":"10.1086/724580","DOIUrl":"https://doi.org/10.1086/724580","url":null,"abstract":"<p><p>AbstractThe interstitial environment of marine sediments is a complex network of voids and pores that is inhabited by a diverse and abundant fauna. Animals living within these interstitial spaces show widespread functional adaptations to this environment and have developed many strategies for moving and navigating through small spaces. Interstitial annelids demonstrate a remarkable level of morphologic diversity, and some possess dexterous, filiform palps (tentacle-like appendages common across Annelida). The function(s) of these palps in interstitial spaces has not been closely examined, and we propose that they serve a sensory role in the navigation of interstitial spaces. We investigated the locomotory function of long, dexterous palps in three families of interstitial annelids to determine their role in interstitial navigation. We observed two species of protodrilids (Protodrilidae), <i>Pharyngocirrus eroticus</i> (Saccocirridae), and <i>Protodorvillea recuperata</i> (Dorvilleidae), as they moved through two transparent sand analogs: cyolite and glass beads. All four species of annelids consistently used their palps to probe the interstitial environment while locomoting, and the distance probed with their palps was greater than the distance traveled with their heads, indicating a sensory form of palp-based navigation. The functionality of palps as sensory organs in the interstitial environment raises interesting questions about interstitial navigation and how fauna without appendages map their surroundings. The discovery of this previously undocumented function was possible only through the direct observation of interstitial behavior and emphasizes the importance of developing new techniques to study these animals in more natural habitats.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 1","pages":"51-62"},"PeriodicalIF":1.6,"publicationDate":"2023-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9513630","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Ryan Mullan, Alex D Davis, Tracey T Sutton, Sönke Johnsen
{"title":"An Investigation into the Mechanism Mediating Counterillumination in Myctophid Fishes (Myctophidae).","authors":"Ryan Mullan, Alex D Davis, Tracey T Sutton, Sönke Johnsen","doi":"10.1086/724803","DOIUrl":"https://doi.org/10.1086/724803","url":null,"abstract":"<p><p>AbstractCounterillumination is a camouflage strategy employed primarily by mesopelagic fishes, sharks, crustaceans, and squid, which use ventral bioluminescence to obscure their silhouettes when viewed from below. Although certain counterilluminating species have been shown to control the intensity of their ventral emissions to match the background downwelling light, the feedback mechanism mediating this ability is poorly understood. One proposed mechanism involves the presence and use of eye-facing photophores that would allow simultaneous detection and comparison of photophore emissions and downwelling solar light. Eye-facing photophores have been found in at least 34 species of counterilluminating stomiiform fishes and the myctophid <i>Tarletonbeania crenularis</i>. Here, we examined nine phylogenetically spaced myctophid species for eye-facing photophores to assess whether this mechanism is as prevalent in this group as it is in the Stomiiformes. First, microcomputed tomography imaging data were collected for each species, and three-dimensional reconstructions of the fishes were developed to identify potential eye-facing photophores. The fishes were then dissected under a stereomicroscope to confirm the presence of all identified photophores, probe for any photophores missed in the reconstruction analysis, and determine the orientation of the photophores' emissions. Although photophores were identified near the orbits of all species examined, none of the fishes' photophores directed light into their orbits, suggesting that myctophids may regulate bioluminescence through an alternative mechanism.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 1","pages":"63-69"},"PeriodicalIF":1.6,"publicationDate":"2023-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9891758","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Fundamental Niche Narrows through Larval Stages of a Filter-Feeding Marine Invertebrate.","authors":"Emily L Richardson, Dustin J Marshall","doi":"10.1086/725151","DOIUrl":"https://doi.org/10.1086/725151","url":null,"abstract":"<p><p>AbstractOntogenetic niche theory predicts that resource use should change across complex life histories. To date, studies of ontogenetic shifts in food niches have mainly focused on a few systems (<i>e.g.</i>, fish), with less attention on organisms with filter-feeding larval stages (<i>e.g.</i>, marine invertebrates). Recent studies suggest that filter-feeding organisms can select specific particles, but our understanding of whether niche theory applies to this group is limited. We characterized the fundamental niche (<i>i.e.</i>, feeding proficiency) by examining how niche breadth changes across the larval stages of the filter-feeding marine polychaete <i>Galeolaria caespitosa</i>. Using a no-choice experimental design, we measured feeding rates of trochophore, intermediate-stage, and metatrochophore larvae on the prey phytoplankton species <i>Nannochloropsis oculata</i>, <i>Tisochrysis lutea</i>, <i>Dunaliella tertiolecta</i>, and <i>Rhodomonas salina</i>, which vary 10-fold in size, from the smallest to the largest. We formally estimated Levins's niche breadth index to determine the relative proportions of each species in the diet of the three larval stages and also tested how feeding rates vary with algal species and stage. We found that early stages eat all four algal species in roughly equal proportions, but niche breadth narrows during ontogeny, such that metatrochophores are feeding specialists relative to early stages. We also found that feeding rates differed across phytoplankton species: the medium-sized cells (<i>Tisochrysis</i> and <i>Dunaliella</i>) were eaten most, and the smallest species (<i>Nannochloropsis</i>) was eaten the least. Our results demonstrate that ontogenetic niche theory describes changes in fundamental niche in filter feeders. An important next step is to test whether the realized niche (<i>i.e.</i>, preference) changes during the larval phase as well.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 1","pages":"25-34"},"PeriodicalIF":1.6,"publicationDate":"2023-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9891760","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Increasing Temperature Results in Higher Allocation of Energy to Protein Synthesis in Sea Urchin Larvae (<i>Lytechinus pictus</i>).","authors":"Melissa B DellaTorre, Donal T Manahan","doi":"10.1086/723369","DOIUrl":"https://doi.org/10.1086/723369","url":null,"abstract":"<p><p>AbstractIt is well established that metabolic processes change with temperature and size. Yet the underlying physiological mechanisms are less well understood regarding how such processes covary within a species and particularly so for developmental stages. Physiological analysis of larvae of the sea urchin <i>Lytechinus pictus</i> revealed that protein was the major biochemical substrate supporting metabolism. The complex dynamics of protein synthesis, turnover, and accretion changed during growth, showing a sevenfold decrease in the ratio of protein accretion to protein synthesis (protein depositional efficiency). To test hypotheses of physiological variation with rising temperature, larvae were reared over a temperature range experienced by this species in its ambient habitat. The thermal sensitivity of protein synthesis was greater than respiration (thermal sensitivity values of 3.7 and 2.4, respectively). Bioenergetic calculations revealed a disproportionate increase in energy allocation toward protein synthesis with rising temperature. These differential temperature sensitivities result in metabolic trade-offs of energy acquisition and expenditure, thereby altering physiological homeostasis. Such insights are of value for improving predictions about limits of biological resilience in a warming ocean.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 1","pages":"35-50"},"PeriodicalIF":1.6,"publicationDate":"2023-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9891764","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Heather Glon, Vreni Häussermann, Paul E Brewin, Paul Brickle, Sungsik Kong, Megan L Smith, Marymegan Daly
{"title":"There and Back Again: The Unexpected Journeys of <i>Metridium</i> de Blainville, 1824 between the Old Oceans and throughout the Modern World.","authors":"Heather Glon, Vreni Häussermann, Paul E Brewin, Paul Brickle, Sungsik Kong, Megan L Smith, Marymegan Daly","doi":"10.1086/723800","DOIUrl":"https://doi.org/10.1086/723800","url":null,"abstract":"<p><p>AbstractMembers of the sea anemone genus <i>Metridium</i> are abundant in temperate rocky habitats and fouling communities. Their biogeographic history is expected to reflect changes in currents and habitats that have influenced benthic communities, such as the climate-influenced changes that occurred during the Last Glacial Maximum. More recently, however, anthropogenic influences such as shipping transportation and the creation of artificial habitat have altered and affected the composition of modern-day marine communities. Here we use sequence-capture data to examine the genetic structure of <i>Metridium</i> across its shallow-water distribution to (1) evaluate species boundaries within <i>Metridium</i>, (2) elucidate the dispersal history of <i>Metridium</i> between and among oceans, and (3) assess the influence of anthropogenic movement on modern-day populations. We find strong evidence for two species within <i>Metridium</i>: <i>M. farcimen</i> and <i>M. senile</i>. Dispersal from the Pacific to the Atlantic included a subsequent isolation of a small population in or above the Bering Sea, which has presumably moved southward. Within the native range of <i>M. senile</i>, admixture is prevalent even between oceans as a result of anthropogenic activities. The nonnative populations in Chile and the Falkland Islands came from at least two distinct introduction events originating from both coasts of the United States in the North Pacific and North Atlantic Oceans. Hybridization between <i>M. senile</i> and <i>M. farcimen</i> is documented as occurring in anthropogenically influenced habitats. The heavy influence from anthropogenic activities will continue to impact our understanding of marine organisms, particularly within the native range and for those that are easily transported across long distances.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":"244 1","pages":"9-24"},"PeriodicalIF":1.6,"publicationDate":"2023-02-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"9891761","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}