Biological Bulletin最新文献

{"title":"Progress Toward Complete Life-Cycle Culturing of the Endangered Sunflower Star, <i>Pycnopodia helianthoides</i>.","authors":"J Hodin,&nbsp;A Pearson-Lund,&nbsp;F P Anteau,&nbsp;P Kitaeff,&nbsp;S Cefalu","doi":"10.1086/716552","DOIUrl":"https://doi.org/10.1086/716552","url":null,"abstract":"<p><p>AbstractUntil recently, the sunflower star, <i>Pycnopodia helianthoides</i>, was a dominant and common predator in a wide variety of benthic habitats in the northeast Pacific. Then, in 2013, its populations began to plummet across its entire range as a result of the spread of a phenomenon known as sea star wasting disease, or sea star wasting. Although dozens of sea star species were impacted by this wasting event, <i>P. helianthoides</i> seems to have suffered the greatest losses and is now listed by the International Union for the Conservation of Nature as the first critically endangered sea star. In order to learn more about the life history of this endangered predator and to explore the potential for its restoration, we have initiated a captive rearing program to attempt complete life-cycle (egg-to-egg) culture for <i>P. helianthoides</i>. We report our observations on holding and distinguishing individual adults, reproductive seasonality, larval development, inducers of settlement, and early juvenile growth and feeding. These efforts will promote and help guide conservation interventions to protect remaining populations of this species in the wild and facilitate its ultimate return.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39899627","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":"Cloning and Selfing Affect Population Genetic Variation in Simulations of Outcrossing, Sexual Sea Stars.","authors":"Michael W Hart,&nbsp;Vanessa I Guerra,&nbsp;Jonathan D Allen,&nbsp;Maria Byrne","doi":"10.1086/717293","DOIUrl":"https://doi.org/10.1086/717293","url":null,"abstract":"<p><p>AbstractMany sea stars are well known for facultative or obligate asexual reproduction in both the adult and larval life-cycle stages. Some species and lineages are also capable of facultative or obligate hermaphroditic reproduction with self-fertilization. However, models of population genetic variation and empirical analyses of genetic data typically assume only sexual reproduction and outcrossing. A recent reanalysis of previously published empirical data (microsatellite genotypes) from two studies of one of the most well-known sea star species (the crown-of-thorns sea star; <i>Acanthaster</i> sp.) concluded that cloning and self-fertilization in that species are rare and contribute little to patterns of population genetic variation. Here we reconsider that conclusion by simulating the contribution of cloning and selfing to genetic variation in a series of models of sea star demography. Simulated variation in two simple models (analogous to previous analyses of empirical data) was consistent with high rates of cloning or selfing or both. More realistic scenarios that characterize population flux in sea stars of ecological significance, including outbreaks of crown-of-thorns sea stars that devastate coral reefs, invasions by <i>Asterias amurensis</i>, and epizootics of sea star wasting disease that kill <i>Pisaster ochraceus</i>, also showed significant but smaller effects of cloning and selfing on variation within subpopulations and differentiation between subpopulations. Future models or analyses of genetic variation in similar study systems might benefit from simulation modeling to characterize possible contributions of cloning or selfing to genetic variation in population samples or to understand the limits on inferring the effects of cloning or selfing in nature.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39810490","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":"Echidnas of the Sea: The Defensive Behavior of Juvenile and Adult Crown-of-Thorns Sea Stars.","authors":"Dione J Deaker,&nbsp;Regina Balogh,&nbsp;Symon A Dworjanyn,&nbsp;Benjamin Mos,&nbsp;Maria Byrne","doi":"10.1086/716777","DOIUrl":"https://doi.org/10.1086/716777","url":null,"abstract":"<p><p>AbstractCrown-of-thorns sea stars are one of the most ecologically important tropical marine invertebrates, with boom-bust population dynamics that influence the community structure of coral reefs. Although predation is likely to influence the development of population outbreaks, little is known about the defensive behavior of crown-of-thorns sea stars. Righting behavior after being overturned, a key defensive response in echinoderms, was investigated for the newly settled herbivorous juvenile, the corallivorous juvenile, and adult stages of crown-of-thorns sea stars. The average righting time of the newly settled juveniles (0.3-1.0-mm diameter) was 2.74 minutes. For the coral-eating juveniles (15-55-mm diameter), the righting time (mean = 6.24 min) was faster in larger juveniles, and the mean righting time of the adults was 6.28 minutes. During righting and in response to being lifted off of the substrate, the juveniles and adults exhibited an arm curling response, during which their arms closed over their oral side, often forming a spine ball, a feature not known for other asteroids. The righting and curling responses of the corallivorous juveniles were influenced by the presence of a natural enemy, a coral guard crab, which caused the juveniles to spend more time with their arms curled. These behaviors indicate that crown-of-thorns sea stars use their spines to protect the soft tissue of their oral side. The highly defended morphology and behavioral adaptations of crown-of-thorns sea stars are likely to have evolved as antipredator mechanisms. This points to the potential importance of predators in regulating their populations, which may have decreased in recent times due to fishing, a factor that may contribute to outbreaks.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39899623","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":"The Waiting Stage, Prolonged Residency in Nursery Habitats by Juveniles of the Predatory Sea Star <i>Marthasterias glacialis</i>.","authors":"Maria Byrne,&nbsp;Dan Minchin,&nbsp;Matthew Clements,&nbsp;Dione J Deaker","doi":"10.1086/715843","DOIUrl":"https://doi.org/10.1086/715843","url":null,"abstract":"<p><p>AbstractGrowth and recruitment of the sea star <i>Marthasterias glacialis</i> was followed over six years in Lough Hyne, southwest Ireland. Juveniles from a 2-mm radius were found on algae at <1-2-m depth following what appeared to be gregarious larval settlement. Data from Lough Hyne and Mulroy Bay (northwest Ireland) indicated that algal habitat serves as a nursery area for juveniles of <i>M. glacialis</i>. Successive size frequency modes of the juveniles at Lough Hyne indicated slow growth over 6 years, to a mean radius of 20 mm. The absence of additional recruitment allowed monitoring of a discrete population. Recruits in the nursery habitat over the six years remained as waiting stage juveniles, a Peter Pan group with delayed maturity subsisting on a diet of epibionts. An initial sharp decline in numbers indicated post-settlement mortality, with subsequent decline likely due to migration to the adjacent shelly habitat, where subadult <i>M. glacialis</i> (30-70-mm radius) lives. In this habitat, <i>M. glacialis</i> preys on small bivalves and eventually joins the adult (maximum radius = 280 mm) population on open sediment, where it feeds on large bivalves. Size frequency distributions of the juveniles and adults showed growth over the six years, with the waiting stage sea stars slowly merging in size with the adult population. It appears that the supply of new individuals into the adult population may take place six or more years following settlement. Strong connectivity between life stage habitats and prolonged recruitment into the adult population may contribute to balanced exploitation of infaunal prey.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-12-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39899624","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":"Receptor Tyrosine Kinases ror1/2 and ryk Are Co-expressed with Multiple Wnt Signaling Components During Early Development of Sea Urchin Embryos.","authors":"C Ka, S Gautam, S R Marshall, L P Tice, M Martinez-Bartolome, J L Fenner, R C Range","doi":"10.1086/715237","DOIUrl":"10.1086/715237","url":null,"abstract":"<p><p>AbstractA combination of receptors, co-receptors, and secreted Wnt modulators form protein complexes at the cell surface that activate one or more of the three different Wnt signaling pathways (Wnt/<i>β</i>-catenin, Wnt/JNK, and Wnt/Ca²⁺). Two or more of these pathways are often active in the same cellular territories, forming Wnt signaling networks; however, the molecular mechanisms necessary to integrate information from these pathways in these situations are unclear in any <i>in vivo</i> model system. Recent studies have implicated two Wnt binding receptor tyrosine kinases, receptor tyrosine kinase-like orphan receptor (Ror) and related-to-receptor tyrosine kinase (Ryk), in the regulation of canonical and non-canonical Wnt signaling pathways, depending on the context; however, the spatiotemporal expression of these genes in relation to Wnt signaling components has not been well characterized in most deuterostome model systems. Here we use a combination of phylogenetic and spatiotemporal gene expression analyses to characterize Ror and Ryk orthologs in sea urchin embryos. Our phylogenetic analysis indicates that both <i>ror1/2</i> and <i>ryk</i> originated as single genes from the metazoan ancestor. Expression analyses indicate that <i>ror1/2</i> and <i>ryk</i> are expressed in the same domains of many Wnt ligands and Frizzled receptors essential for the specification and patterning of germ layers along the early anterior-posterior axis. In addition, both genes are co-expressed with Wnt signaling components in the gut, ventral ectoderm, and anterior neuroectoderm territories later in development. Together, our results indicate that Ror and Ryk have a complex evolutionary history and that their spatiotemporal expression suggests that they could contribute to the complexity of Wnt signaling in early sea urchin embryogenesis.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":2.1,"publicationDate":"2021-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11257382/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"10851223","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":4,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}

{"title":"The Specialist Marine Herbivore <i>Elysia papillosa</i> Grows Faster on a Less Utilized Algal Diet.","authors":"Kourtney Barber,&nbsp;Michael Middlebrooks,&nbsp;Susan Bell,&nbsp;Sidney Pierce","doi":"10.1086/716508","DOIUrl":"https://doi.org/10.1086/716508","url":null,"abstract":"<p><p>AbstractMany small specialist herbivores utilize their food resources both for nutrition and as a structural refuge or resource. Trophic linkage cannot solely be inferred from physical association of herbivores with a potential food item, because herbivores may temporarily inhabit algae or plants on which they do not feed. <i>Elysia papillosa</i>, a small sacoglossan sea slug, consumes and sequesters chloroplasts from the siphonaceous, chlorophytic alga <i>Penicillus capitatus</i>; it also maintains moderate densities on this alga. Recently, <i>E. papillosa</i> was also infrequently found in association with the alga <i>Penicillus lamourouxii</i>, which displays density similar to that of <i>P. capitatus</i>. After collecting <i>E. papillosa</i> from each of the two algal species from a shallow-water site along the west central coast of Florida, we used DNA barcoding of the <i>rbcL</i> gene sequences in order to determine whether the slug was consuming both algal species. The molecular data indicated that <i>E. papillosa</i> consumed and sequestered chloroplasts from the same algal species from which they were collected. A laboratory feeding experiment tested whether algal diet (<i>P. capitatus</i> or <i>P. lamourouxii</i>) had an impact on slug growth rate as measured by change in body size (mm). After 3 weeks <i>E. papillosa</i> fed <i>P. lamourouxii</i> achieved a mean body length that was 1.5-2 times that recorded for slugs fed <i>P. capitatus</i>, but maximum growth depended on the original field host. Thus, while the highest densities of <i>E. papillosa</i> in the field occurred on <i>P. capitatus</i>, slugs grew much faster on <i>P. lamourouxii</i> in the laboratory. The observed association of <i>E. papillosa</i> with <i>P. capitatus</i> must be related to other factors, such as foraging efficiency, algal morphology, algal biochemistry, or algal suitability as a refuge.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39562933","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":"Kelp Morphology and Herbivory Are Maintained Across Latitude Despite Geographic Shift in Kelp-Wounding Herbivores.","authors":"Nicholas P Burnett, Eric J Armstrong, Rosemary Romero, Charlotte C Runzel, Richelle L Tanner","doi":"10.1086/715039","DOIUrl":"10.1086/715039","url":null,"abstract":"<p><p>AbstractHerbivores can drastically alter the morphology of macroalgae by directly consuming tissue and by inflicting structural wounds. Wounds can result in large amounts of tissue breaking away from macroalgae, amplifying the damage initially caused by herbivores. Herbivores that commonly wound macroalgae often occur over only a portion of a macroalga's lifespan or geographic range. However, we know little about the influence of these periodic or regional occurrences of herbivores on the large-scale seasonal and geographical patterns of macroalgal morphology. We used the intertidal kelp <i>Egregia menziesii</i> to investigate how the kelp's morphology and the prevalence of two prominent kelp-wounding herbivores (limpets and amphipods) changed over two seasons (spring and summer) and over the northern extent of the kelp's geographic range (six sites from central California to northern Washington). Wounds from limpets and amphipods often result in the kelp's fronds being pruned (intercalary meristem broken away), so we quantified kelp size (combined length of all fronds) and pruning (proportion of broken fronds). We found similar results in each season: herbivores were most likely to occur on large, pruned kelp regardless of site; and limpets were the dominant herbivore at southern sites, while amphipods were dominant at northern sites. Despite the geographic shift in the dominant herbivore, kelp had similar levels of total herbivore prevalence (limpets and/or amphipods) and similar morphologies across sites. Our results suggest that large-scale geographic similarities in macroalgal wounding, despite regional variation in the herbivore community, can maintain similar macroalgal morphologies over large geographic areas.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39562930","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":"Bivalves as Biological Sieves: Bioreactivity Pathways of Microplastics and Nanoplastics.","authors":"Amy Huffman Ringwood","doi":"10.1086/716259","DOIUrl":"https://doi.org/10.1086/716259","url":null,"abstract":"<p><p>AbstractOceanic and coastal sampling programs have indicated extensive plastic pollution of marine habitats and revealed the need for understanding the scope and potential impacts of plastics on marine organisms. Sampling regimes for macroplastics (>5 mm) that can be visually collected for quantification and characterization in marine habitats provide valuable environmental data for the larger plastics. But less is known about the scope or potential impacts of small micron- and nano-sized bits of plastic that result from weathering of macroplastics and inputs of manufactured particles that could profoundly affect marine invertebrates, especially suspension feeders. Essential fundamental information about bivalve biology along with current research and reviews on microplastics, nanoplastics, and engineered nanoparticles were integrated to discuss how filter-feeding bivalves can serve as valuable bioindicators of plastic pollution. Bivalves can serve as important bioaccumulators of plastic particles and exhibit processing pathways that serve as biological sieves. Mesoplastics (1-5 mm) and large microplastics (>25 <i>µ</i>m) will have a relatively short transit time (hours to days) and will primarily be concentrated in biodeposits (pseudofeces and feces). Small microplastics (<25 <i>µ</i>m) and nanoplastics (<1 <i>µ</i>m) are more likely to be accumulated in digestive gland tissues and cells, and also hemocytes, and will have longer retention times. Lysosomes are a common target organelle for uptake and toxicity in both of these cell types. Therefore, bivalves can potentially act as biological sieves for characterizing relative environmental exposures and bioreactivity of microplastics and nanoplastics, based on critical particle capture and processing pathways. This framework highlights the importance of developing diagnostic approaches to characterize potential environmental risks associated with plastic particles as well as potential interactions with other anthropogenic pollutants.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39562931","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":"Linear Dominance Hierarchies in Female Grass Shrimp <i>Palaemon pugio</i>.","authors":"Samuel D Rappaport,&nbsp;Joshua P Lord","doi":"10.1086/716227","DOIUrl":"https://doi.org/10.1086/716227","url":null,"abstract":"<p><p>AbstractThe grass shrimp <i>Palaemon pugio</i> is an abundant and ecologically important species in estuarine habitats in the northwest Atlantic and is commonly used as an indicator species for environmental contamination, but little is known about its behavior. We examined aggression and dominance in <i>P. pugio</i> by using experimental arenas and groups of five shrimp that were observed an hour at a time for three days in the laboratory. Female shrimp showed high levels of initial aggression that quickly decreased over time, suggesting the formation of a dominance hierarchy. The dominance hierarchy between groups of females appeared linear, with shrimp at five distinct ranks in most replicates and higher-ranked individuals dominating lower-ranked ones. Dominance was significantly correlated with cheliped size but not body size, suggesting that larger chelipeds in female <i>P. pugio</i> may have evolved as a tool to establish dominance, perhaps to gain access to shelter in salt marshes, seagrass beds, or oyster reefs. Grass shrimp are preyed upon by a wide range of estuarine fish, and females are especially vulnerable; so securing access to shelter may provide a major selective advantage, with the dominance hierarchy evolving to save energy through a long-term reduction in fighting over resources.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39562929","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":"<i>N</i>-Acetyl Neuraminic Acid (NANA) Activates L-Type Calcium Channels on Isolated Tentacle Supporting Cells of the Sea Anemone (<i>Aiptasia pallida</i>).","authors":"V Haktan Ozacmak,&nbsp;Aida Ricardo Arrieta,&nbsp;Glyne U Thorington,&nbsp;David A Hessinger","doi":"10.1086/715844","DOIUrl":"https://doi.org/10.1086/715844","url":null,"abstract":"<p><p>AbstractSensory receptors control nematocyst discharge on sea anemone tentacles. Micromolar <i>N</i>-acetylated sugars (<i>e.g.</i>, <i>N</i>-acetyl neuraminic acid [NANA]) bind chemoreceptors on ectodermal supporting cells and predispose adjacent nematocyst discharge in response to mechanical contact <i>via</i> a cyclic adenosine monophosphate (cAMP)-dependent sensitization pathway, while higher NANA levels dose-dependently desensitize. Recent evidence implicates L-type calcium channels in desensitizing the pathway in aconitate sea anemones <i>Aiptasia pallida</i> (also known as <i>Exaiptasia diaphana</i>). We, therefore, hypothesize that NANA activates calcium influx <i>via</i> L-type calcium channels. We demonstrate a dose-dependent, NANA-activated ⁴⁵Ca influx into dissociated ectodermal cells isolated from <i>A. pallida</i> tentacles, with maximal influx occurring at desensitizing concentrations of NANA. The L-type calcium channel inhibitors nifedipine, diltiazem, methoxyverapamil, and cadmium blocked NANA-stimulated ⁴⁵Ca influx. Elevated extracellular KCl levels dose-dependently increased nifedipine-sensitive ⁴⁵Ca influx to implicate voltage-gated calcium channels. Forskolin, 8-bromo-cAMP, and the protein kinase A inhibitor H-8 affect NANA-stimulated calcium influx in a manner consistent with activated cAMP-dependent pathway involvement. Because NANA chemoreceptors localize to supporting cells of cnidocyte supporting cell complexes, NANA activation of ⁴⁵Ca influx into isolated tentacle ectodermal cells suggests that L-type calcium channels and NANA chemoreceptors co-localize to supporting cells. Indeed, a fluorescent marker of L-type calcium channels localizes to the apical ectoderm adjacent to nematocysts of live tentacles. We conclude that supporting cell chemoreceptors activate co-localized L-type calcium channels <i>via</i> a cAMP-dependent mechanism in order to initiate desensitization. We suggest that pathway desensitization may conserve nematocysts from excessive discharge during prey capture.</p>","PeriodicalId":55376,"journal":{"name":"Biological Bulletin","volume":null,"pages":null},"PeriodicalIF":1.6,"publicationDate":"2021-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"39563367","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}