Marine Invertebrate Larvae Research Articles

Ocean conditions influence the quality of recruiting benthic marine invertebrate larvae—Insights from fatty acids

AbstractMany marine benthic invertebrates have a pelagic life stage, during which larvae need to accumulate enough reserves to complete metamorphosis to a settled benthic juvenile. Currently, very little is known about how ocean conditions affect quality of the larvae. We studied this for three settlement seasons (2017–2019) by collecting returning Dungeness crab (Metacarcinus magister) megalopae at the Oregon coast and analyzing them for fatty acid biomarkers. We found that the larvae are omnivorous and have versatile diets. The daily larval abundance was positively correlated with larval quality. Despite the relatively high day‐to‐day variation, we found pronounced seasonal and inter‐annual differences in the body condition (size and total fatty acid content) and biomarker composition of megalopae. Especially, the early season recruits of 2017 had lower content of lipids and polyunsaturated fatty acids known to be beneficial to crustaceans. This is likely related to lingering effects of the eastern Pacific marine heat wave (2014–2016) on pelagic communities. The larvae were rich in docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA) with lower levels in benthic juveniles, indicating an ontogenetic diet shift and likely lower availability of DHA and EPA in the benthic environment. The pulsed megalopa recruitment may provide substantial carbon and lipid inputs to the nearshore ecosystem as a form of pelagic subsidy. Our results reveal that ocean conditions may have an effect on the quality of returning larvae, which likely influence their recruitment performance and early juvenile success, and thus potentially also the population size and commercial catch 4 yr later.

Establishment of a new subfamily for the parasitic isopod genus Pleurocryptella (Isopoda: Bopyridae), including recognition of epicaridium larval yolk sacs and description of a new genus and species of hyperparasite

Abstract External yolk sacs in free-living larvae of marine invertebrates are extremely rare, with all reported cases exhibiting yolk that is taken up through connection with the anterior alimentary canal. Herein, we confirm a novel yolk sac connected to the posterior end of the alimentary canal in the first larval stage of species in the bopyrid isopod genus PleurocryptellaBonnier, 1900, all known as ectoparasites in the branchial chambers of squat lobsters. Pleurocryptella poseidon Williams & Boyko sp. nov. infesting the munidopsid Galacantha bellis Henderson, 1885 in the Arabian Sea, is described on the basis of adults and larvae. In common with conspecifics, the new species exhibits a suite of putative “primitive” characters including the presence of oostegites on the sixth and seventh pereomeres of females and maxillipeds and articulated uropods in males. Pleurocryptella poseidon Williams & Boyko sp. nov. differs from other species of Pleurocryptella by characters of body shape, antennae, oostegite 1, pleon, and uropods of females and midventral tubercles, pleomeres, and pleopods of males. The epicaridium larvae have a large posterior, external yolk sac and segmented maxillipeds, a unique set of characters within Epicaridea. In addition to larval and adult characters, molecular data (COI) indicate that the genus is distinct from other members of Bopyridae, so we erect the new subfamily Pleurocryptellinae for it. Pleurocryptella poseidon Williams & Boyko sp. nov. bears a new genus and species of hyperparasitic isopod that is herein described based on its cryptoniscus stage. A review of epicaridium larval morphology and a key to the species of Pleurocryptella are provided.

Evaluation of light traps for sampling lobster larvae in the German Bight, North Sea

Biological monitoring of planktonic animals is greatly dependent on the deployment of traps. A variety of specialized traps have been designed for surface plankton and vertebrates. However, certain groups, such as planktonic larvae of benthic marine invertebrates remain underrepresented in sampling efforts. Catching them has proven to be more challenging because of their size, swimming ability, location, and abundance. In the present study a successful light trap for sampling American lobster larvae in New Brunswick, Canada, is evaluated on the island of Helgoland (German Bight, North Sea). Our results showed the traps were successful in catching larvae in laboratory experiments but were unable to catch European lobster larvae in the field. Traps deployed in the field were successful in capturing other benthic and pelagic zooplankton predominantly consisting of crustaceans from the orders: Cumacea, Amphipoda, Mysida and Isopoda. The low density of lobster larvae, the island's topography, and their unique photactic response possibly limited the success rate of the light traps. Future research is needed to construct a specialized trap to sample Helgoland's lobster larvae and provide information on the current larval fitness and population numbers.

Making Your Own Luck: Weak Vertical Swimming Improves Dispersal Success for Coastal Marine Larvae

Dispersive early life stages are common in nature. Although many dispersing organisms (“propagules”) are passively moved by outside forces, some improve their chances of successful dispersal through weak movements that exploit the structure of the environment to great effect. The larvae of many coastal marine invertebrates, for instance, swim vertically through the water column to exploit depth-varying currents, food abundance, and predation risk. Several swimming behaviors and their effects on dispersal between habitats are characterized in the literature, yet it remains unclear when and why these behaviors are advantageous. We addressed this gap using a mathematical model of larval dispersal that scored how well behaviors allowed larvae to simultaneously locate habitats, avoid predators, and gather energy. We computed optimal larval behaviors through dynamic programming, and compared those optima against passive floating and three well documented behaviors from the literature. Optimal behaviors often (but not always) resembled the documented ones. However, our model predicted that the behaviors from the literature performed robustly well, if not optimally, across many conditions. Our results shed light on why some larval behaviors are widespread geographically and across species, and underscore the importance of carefully considering the weak movements of otherwise passive propagules when studying dispersal.

Interactive roles of temperature and food availability in predicting habitat suitability for marine invertebrates

Natural variability in habitat characteristics, including their interactions, can affect marine invertebrate development. Controlled laboratory experiments seek to assess responses to such variability. For marine invertebrates, responses to temperature are typically assessed but a continuous gradient of all temperatures that a species may encounter is not frequently used. For planktonic larvae of marine invertebrates, biotic factors such as food availability receive less attention due to difficulty in simulating planktonic biotic interactions in a controlled laboratory setting. Here, a laboratory experiment was used to quantify larval development (growth, pelagic larval duration and survival) of the Atlantic surfclam, Spisula solidissima, in response to a continuous range of temperatures and food (phytoplankton) concentrations, allowing quantification of thermal and food availability niches. A second experiment was conducted to quantify the thermal and food availability niches for recruit (post-settlement) surfclams. These experiments were uniquely designed to inform future climate change-based forecasting and habitat suitability modeling. Larval growth and survival increased with increased food availability, while pelagic larval duration decreased with increased food availability. Larval survival decreased with increased temperature, growth peaked near 22 °C and pelagic larval duration was lowest near 22 °C. For recruits, survival and growth increased with both temperature and food availability, but growth decreased at temperatures >22 °C. Broadly, results suggest potential food limitation for continental shelf bivalve larvae and demonstrate that natural variation in food availability may affect thermal tolerances. Results also suggest that throughout the range of the surfclam, high food and moderate temperature areas such as New York Bight and Georges Bank are ideal for larvae and early recruits, whereas low food and high temperature areas, including continental shelf waters in the southern Middle Atlantic Bight, are suboptimal for early life stages of surfclams. This framework may be used for habitat suitability modeling, from an energetic perspective, for other marine invertebrate taxa.

Metabolic Regulation of Copper Toxicity during Marine Mussel Embryogenesis.

The development of new tools for assessing the health of cultured shellfish larvae is crucial for aquaculture industries to develop and refine hatchery methodologies. We established a large-volume ecotoxicology/health stressor trial, exposing mussel (Perna canaliculus) embryos to copper in the presence of ethylenediaminetetraacetic acid (EDTA). GC/MS-based metabolomics was applied to identify potential biomarkers for monitoring embryonic/larval health and to characterise mechanisms of metal toxicity. Cellular viability, developmental abnormalities, larval behaviour, mortality, and a targeted analysis of proteins involved in the regulation of reactive oxygen species were simultaneously evaluated to provide a complementary framework for interpretative purposes and authenticate the metabolomics data. Trace metal analysis and speciation modelling verified EDTA as an effective copper chelator. Toxicity thresholds for P. canaliculus were low, with 10% developmental abnormalities in D-stage larvae being recorded upon exposure to 1.10 μg·L-1 bioavailable copper for 66 h. Sublethal levels of bioavailable copper (0.04 and 1.10 μg·L-1) caused coordinated fluctuations in metabolite profiles, which were dependent on development stage, treatment level, and exposure duration. Larvae appeared to successfully employ various mechanisms involving the biosynthesis of antioxidants and a restructuring of energy-related metabolism to alleviate the toxic effects of copper on cells and developing tissues. These results suggest that regulation of trace metal-induced toxicity is tightly linked with metabolism during the early ontogenic development of marine mussels. Lethal-level bioavailable copper (50.3 μg·L-1) caused severe metabolic dysregulation after 3 h of exposure, which worsened with time, substantially delayed embryonic development, induced critical oxidative damage, initiated the apoptotic pathway, and resulted in cell/organism death shortly after 18 h of exposure. Metabolite profiling is a useful approach to (1) assess the health status of marine invertebrate embryos and larvae, (2) detect early warning biomarkers for trace metal contamination, and (3) identify novel regulatory mechanisms of copper-induced toxicity.

Having cake and eating too: The benefits of an intermediate larval form in a brittle star Amphiodia sp. opaque (Ophiuroidea).

Most marine invertebrate larvae either obligately feed or depend on maternally provided reserves during planktonic development. A small number of species have the capacity to do both, in a mode of development known as facultative planktotrophy. We describe facultative feeding in a larva from the Oregon coast, and identify it as being an undescribed species in the genus Amphiodia, which we refer to as Amphiodia sp. opaque. We quantified the effects of food on larval and juvenile quality by culturing larvae, collected as embryos, with and without microalgal food at 15°C. The resulting juveniles were monitored under conditions of starvation. A cohort of juveniles of larvae caught as plankton was subjected to the same starvation treatment for comparison with our laboratory-reared larvae. We observed benefits to offspring that received food: larvae provided with microalgae developed more quickly and metamorphosed at higher rates. Furthermore, juveniles resulting from fed larvae were larger and were able to avoid starvation for longer after metamorphosis. Our results varied across two experimental years, suggesting that provisions provided by parents vary between populations and years. Juveniles from planktonic larvae exhibited sizes not statistically different from larvae cultured in the absence of food, but died from starvation more quickly.

Multisensory integration by polymodal sensory neurons dictates larval settlement in a brainless cnidarian larva.

Multisensory integration (MSI) combines information from more than one sensory modality to elicit behaviours distinct from unisensory behaviours. MSI is best understood in animals with complex brains and specialized centres for parsing different modes of sensory information, but dispersive larvae of sessile marine invertebrates utilize multimodal environmental sensory stimuli to base irreversible settlement decisions on, and most lack complex brains. Here, we examined the sensory determinants of settlement in actinula larvae of the hydrozoan Ectopleura crocea (Cnidaria), which possess a diffuse nerve net. A factorial settlement study revealed that photo-, chemo- and mechanosensory cues each influenced the settlement response in a complex and hierarchical manner that was dependent on specific combinations of cues, an indication of MSI. Additionally, sensory gene expression over development peaked with developmental competence to settle, which in actinulae, requires cnidocyte discharge. Transcriptome analyses also highlighted several deep homological links between cnidarian and bilaterian mechano-, chemo-, and photosensory pathways. Fluorescent in situ hybridization studies of candidate transcripts suggested cellular partitioning of sensory function among the few cell types that comprise the actinula nervous system, where ubiquitous polymodal sensory neurons expressing putative chemo- and photosensitivity interface with mechanoreceptive cnidocytes. We propose a simple multisensory processing circuit, involving polymodal chemo/photosensory neurons and mechanoreceptive cnidocytes, that is sufficient to explain MSI in actinulae settlement. Our study demonstrates that MSI is not exclusive to complex brains, but likely predated and contextualized their evolution.

Stage-Specific Transcriptomes of the Mussel Mytilus coruscus Reveals the Developmental Program for the Planktonic to Benthic Transition.

Many marine invertebrate larvae undergo complex morphological and physiological changes during the planktonic-benthic transition (a.k.a. metamorphosis). In this study, transcriptome analysis of different developmental stages was used to uncover the molecular mechanisms underpinning larval settlement and metamorphosis of the mussel, Mytilus coruscus. Analysis of highly upregulated differentially expressed genes (DEGs) at the pediveliger stage revealed enrichment of immune-related genes. The results may indicate that larvae co-opt molecules of the immune system to sense and respond to external chemical cues and neuroendocrine signaling pathways forecast and trigger the response. The upregulation of adhesive protein genes linked to byssal thread secretion indicates the anchoring capacity required for larval settlement arises prior to metamorphosis. The results of gene expression support a role for the immune and neuroendocrine systems in mussel metamorphosis and provide the basis for future studies to disentangle gene networks and the biology of this important lifecycle transformation.

The rangeomorph Pectinifrons abyssalis: Hydrodynamic function at the dawn of animal life

Rangeomorphs are among the oldest putative eumetazoans known from the fossil record. Establishing how they fed is thus key to understanding the structure and function of the earliest animal ecosystems. Here, we use computational fluid dynamics to test hypothesized feeding modes for the fence-like rangeomorph Pectinifrons abyssalis, comparing this to the morphologically similar extant carnivorous sponge Chondrocladia lyra. Our results reveal complex patterns of flow around P.abyssalis unlike those previously reconstructed for any other Ediacaran taxon. Comparisons with C. lyra reveal substantial differences between the two organisms, suggesting they converged on a similar fence-like morphology for different functions. We argue that the flow patterns recovered for P.abyssalis do not support either a suspension feeding or osmotrophic feeding habit. Instead, our results indicate that rangeomorph fronds may represent organs adapted for gas exchange. If correct, this interpretation could require a dramatic reinterpretation of the oldest macroscopic animals.

AMPK Promotes Larval Metamorphosis of Mytilus coruscus.

Metamorphosis is a critical process in the transition from planktonic life to benthic life for marine invertebrates, which is accompanied by a large amount of energy consumption. Previous studies have proved that AMP-activated protein kinase (AMPK), as a vital energy regulator, plays a prominent role in mediating the growth and development of terrestrial animals. However, its function in the growth and development of marine invertebrates, especially in metamorphosis, remains elusive. This study explored the function of AMPK in the larval metamorphosis of Mytilus coruscus. The full-length cDNA of AMPK genes in M. coruscus was cloned and characterized, which is composed of three subunits, McAMPKα, McAMPKβ, and McAMPKγ. Pharmacological tests demonstrated that through the application of an AMPK activator, AMP substantially enhanced the larval metamorphosis rate (p < 0.05). By contrast, the larval metamorphosis rate decreased significantly after being treated with the AMPK inhibitor Compound C (p < 0.05). McAMPK gene knock-down resulted in a reduction in McAMPK gene expression (p < 0.05), and the larval metamorphosis of M. coruscus was significantly restrained (p < 0.05). These results indicated that AMPK signaling is vital in the larval metamorphosis of M. coruscus, which advances further understanding in exploring the molecular mechanisms in the metamorphosis of marine invertebrate larvae.

Oxygen and irradiance constraints on visual habitat in a changing ocean: The luminoxyscape

Oxygen and irradiance constraints on visual habitat in a changing ocean: The luminoxyscape

Microplastics impede larval urchin selective feeding.

Microplastics are emergent threats to marine organisms as ingestion can cause a multitude of physiological problems. Suspension feeders, including marine invertebrate larvae, are particularly susceptible to ingesting microplastics due to similarities in physical appearance to algal cells. Larval feeding involves multiple stages: the capture and subsequent selection of particles followed by ingestion from the mouth to the stomach, digestion, and finally, egestion. Yet, little is known about which aspect of the feeding process is disrupted by microplastics. Here, we determine if prior exposure to microplastics alters the feeding behavior of the larval sea urchin Heliocidaris crassispina. We conducted two experiments: a food handling experiment studied larval survival, growth, and time required to fill and vacate the stomach; and a particle selection experiment analyzed changes in the ability of the larvae to selectively ingest algal cells over microplastics. In both experiments, larvae were pre-exposed to algae only (control), the addition of 10 μm polystyrene beads at 1 bead mL-1 or 1000 beads mL-1 until 3- or 7-days post-fertilization. Previous exposure to microplastics lengthened stomach filling time and impaired particle selection. While there was no significant change in survivorship and larval arm length, these sub-lethal impacts on larval feeding likely have more severe ramifications in vivo where food is limited, and thus, potentially threaten post-settlement success.

No evidence for temporally balanced selection on larval Pacific oysters Crassostrea gigas: a comment on Durland et al. (2021).

No evidence for temporally balanced selection on larval Pacific oysters Crassostrea gigas: a comment on Durland et al. (2021).

Diacylglycerol, PKC and MAPK signaling initiate tubeworm metamorphosis in response to bacteria

External environmental cues can have significant impacts on the timing and outcomes of animal development. For the swimming larvae of many marine invertebrates, the presence of specific surface-bound bacteria are important cues that help larvae identify a suitable location on the sea floor for metamorphosis and adult life. While metamorphosis in response to bacteria occurs in diverse animals from across the animal tree of life, we know little about the signal transduction cascades stimulated at the onset of metamorphosis upon their interaction with bacteria. The metamorphosis of a model tubeworm, Hydroides elegans, is triggered by the bacterium Pseudoalteromonas luteoviolacea which produces a stimulatory protein called Mif1. In this work, we define three key nodes in a signaling cascade promoting Hydroides metamorphosis in response to Mif1. Using metabolomic profiling, we find that the stimulation of Hydroides larvae by P. luteoviolacea leads to an increase in diacylglycerol during the initiation of metamorphosis, and that Mif1 is necessary for this upregulation. Genomic and pharmacological examination suggests that diacylglycerol triggers a phosphotransferase signaling cascade involving Protein Kinase C (PKC) and Mitogen-Activated Protein Kinase (MAPK), to induce Hydroides metamorphosis. Additionally, Mif1 activates the expression of two nuclear hormone receptors, HeNHR1 and HeNHR2 in the cerebral ganglia of Hydroides larvae. Our results define a post-translational signal transduction pathway mediating bacteria-stimulated metamorphosis in a model invertebrate animal.

Bacterial lipopolysaccharide induces settlement and metamorphosis in a marine larva

How larvae of the many phyla of marine invertebrates find places appropriate for settlement, metamorphosis, growth, and reproduction is an enduring question in marine science. Biofilm-induced metamorphosis has been observed in marine invertebrate larvae from nearly every major marine phylum. Despite the widespread nature of this phenomenon, the mechanism of induction remains poorly understood. The serpulid polychaete Hydroides elegans is a well established model for investigating bacteria-induced larval development. A broad range of biofilm bacterial species elicit larval metamorphosis in H. elegans via at least two mechanisms, including outer membrane vesicles (OMVs) and complexes of phage-tail bacteriocins. We investigated the interaction between larvae of H. elegans and the inductive bacterium Cellulophaga lytica, which produces an abundance of OMVs but not phage-tail bacteriocins. We asked whether the OMVs of C. lytica induce larval settlement due to cell membrane components or through delivery of specific cargo. Employing a biochemical structure–function approach with a strong ecological focus, the cells and OMVs produced by C. lytica were interrogated to determine the class of the inductive compounds. Here, we report that larvae of H. elegans are induced to metamorphose by lipopolysaccharide produced by C. lytica. The widespread prevalence of lipopolysaccharide and its associated taxonomic and structural variability suggest it may be a broadly employed cue for bacterially induced larval settlement of marine invertebrates.

Reduced Oxygen Impairs Photobehavior in Marine Invertebrate Larvae.

AbstractOrganisms in coastal waters experience naturally high oxygen variability and steep oxygen gradients with depth, in addition to ocean deoxygenation. They often undergo diel vertical migration involving a change in irradiance that initiates a visual behavior. Retinal function has been shown to be highly sensitive to oxygen loss; here we assess whether visual behavior (photobehavior) in paralarvae of the squid Doryteuthis opalescens and the octopus Octopus bimaculatus is affected by low oxygen conditions, using a novel behavioral paradigm. Larvae showed an irradiance-dependent, descending photobehavior after extinction of the light stimulus, measured through the change in vertical position of larvae in the chamber. The magnitude of photobehavior was decreased as oxygen was reduced, and the response was entirely gone at <6.4 kPa partial pressure of oxygen (<74.7 μmol kg-1 at 15.3 °C) in D. opalescens paralarvae. Oxygen also affected photobehavior in O. bimaculatus paralarvae. The mean vertical velocity of paralarvae was unaffected by exposure to reduced oxygen, indicating that oxygen deficits selectively affect vision prior to locomotion. These findings suggest that variable and declining oxygen conditions in coastal upwelling areas and elsewhere will impair photobehavior and likely affect the distribution, migration behavior, and survival of highly visual marine species.

Effects of currents, waves, and biofilms on motion and surface contacts by tubeworm larvae swimming above or below surfaces

Larvae of many benthic marine invertebrates swim more slowly than the ambient water flow that carries them past surfaces where they might settle. Competent larvae of the tubeworm Hydroides elegans, abundant early colonists in warm-water fouling communities, were used to determine if active behavior by microscopic larvae carried in flowing water can affect their contacts with surfaces representing early stages of fouling community succession (clean flat surface, flat biofilm, biofilm on worm tubes). We studied larvae in waves and in the unidirectional flow used in earlier studies of larval settlement, and near surfaces above them (like those where fouling organisms recruit) or below them. We videotaped larval motion near surfaces in a small flume in which we mimicked fine-scale flow measured near surfaces in harbors. Swimming larvae within millimeters of surfaces moved up and down while being carried by horizontal flow, enhancing their contact rates with surfaces above and below them compared with dead larvae passively carried by the current. After contact, live larvae ‘bounced’ along the surface, sampling it many times per distance they were carried by the current, whereas dead larvae did not. Thus, active behaviors of larvae of H. elegans, which must touch a biofilmed surface to be stimulated to attach and metamorphose, enhance their contact with and exploration of surfaces in flowing water. These behaviors are effective in unidirectional flow and waves, for surfaces above or below larvae, and for smooth or rough surfaces, all of which are conditions that the larvae of fouling-community animals encounter in harbors.

Origin of marine invertebrate larvae on an Arctic inflow shelf

Many benthic invertebrate taxa possess planktonic early life stages which drift with water currents and contribute to dispersal of the species, sometimes reaching areas beyond the current ranges of the adults. Until recently, it had been difficult to identify planktonic larvae to species level due to lack of distinguishing features, preventing detection of expatriate species. Here, we used DNA metabarcoding of the COI gene to obtain species-level identification of early life stages of benthic invertebrates in zooplankton samples from the Barents Sea and around Svalbard, where, regionally, large volumes of warm Atlantic Water enter the Arctic from the south. We compared the larval community in the water column to the adult community on the seafloor to identify mismatches. In addition, we implemented particle tracking analysis to identify the possible areas of origin of larvae. Our results show that 30-45% of larval taxa—largely polychaetes and nudibranchs—were not local to the sampling area, though most were found nearby in the Barents Sea. In the particle tracking analysis, some larvae originating along the Norwegian coast were capable of reaching the northwest coast of Svalbard within 3 mo, but larvae found east of Svalbard had a more constrained possible area of origin which did not extend to the Norwegian coast. This study highlights largely regional-scale larval connectivity in the Barents Sea but demonstrates the potential for some long-lived larval taxa to travel to Svalbard and the Barents Sea from further south.

Larvae of coastal marine invertebrates enhance their settling success or benefits of planktonic development – but not both – through vertical swimming

The planktonic larvae of many coastal marine invertebrates swim vertically during dispersal to exploit variation in current strength and direction, food abundance and mortality rate throughout the water column and offshore. Prior studies have estimated the effects of vertical swimming upon larval dispersal using mathematical models. However, most such studies consider just a small number of predefined swimming behaviors despite evidence that even seemingly insignificant changes to these behaviors can dramatically alter predictions of larval delivery. Additionally, the concurrent effects of vertical swimming upon predation risk, feeding opportunities and energy budgeting are not well characterized. We used a simple mathematical model of larval dispersal in upwelling‐favorable conditions to investigate how a continuum of swimming behaviors affect these quantities simultaneously. Within this continuum, we identified two categories of successful behaviors. ‘Mean‐onshore' behaviors deliver most larvae to coastal habitats, but offer limited opportunities for feeding and alongshore movement during dispersal. By contrast, ‘mean‐offshore' behaviors deliver fewer larvae to shore, but permit more feeding, alongshore movement, and, potentially, safety from nearshore hazards. No behaviors considered achieved the benefits of both categories. We hypothesize that mean‐onshore behaviors are advantageous for species with non‐feeding larvae or sparse adult populations, while mean‐offshore behaviors are advantageous for species with feeding larvae or crowded adult populations. Our results underscore the importance of considering how behavior interacts with environmental structure and individual biology while studying dispersal in marine and other ecosystems.