A genetically tractable jellyfish model for systems and evolutionary neuroscience.

Jellyfish are radially symmetric organisms without a brain that arose more than 500 million years ago. They achieve organismal behaviors through coordinated interactions between autonomously functioning body parts. Jellyfish neurons have been studied electrophysiologically, but not at the systems level. We introduce Clytia hemisphaerica as a transparent, genetically tractable jellyfish model for systems and evolutionary neuroscience. We generate stable F1 transgenic lines for cell-type-specific conditional ablation and whole-organism GCaMP imaging. Using these tools and computational analyses, we find that an apparently diffuse network of RFamide-expressing umbrellar neurons is functionally subdivided into a series of spatially localized subassemblies whose synchronous activation controls directional food transfer from the tentacles to the mouth. These data reveal an unanticipated degree of structured neural organization in this species. Clytia affords a platform for systems-level studies of neural function, behavior, and evolution within a clade of marine organisms with growing ecological and economic importance.

Two Distinct Bacterial Biofilm Components Trigger Metamorphosis in the Colonial Hydrozoan Hydractinia echinata.

In marine environments, the bacterially induced metamorphosis of larvae is a widespread cross-kingdom communication phenomenon that is critical for the persistence of many marine invertebrates. However, the majority of inducing bacterial signals and underlying cellular mechanisms remain enigmatic. The marine hydroid Hydractinia echinata is a well-known model system for investigating bacterially stimulated larval metamorphosis, as larvae transform into the colonial adult stage within 24 h of signal detection. Although H. echinata has served as a cell biological model system for decades, the identity and influence of bacterial signals on the morphogenic transition remained largely unexplored. Using a bioassay-guided analysis, we first determined that specific bacterial (lyso)phospholipids, naturally present in bacterial membranes and vesicles, elicit metamorphosis in Hydractinia larvae in a dose-response manner. Lysophospholipids, as single compounds or in combination (50 µM), induced metamorphosis in up to 50% of all larvae within 48 h. Using fluorescence-labeled bacterial phospholipids, we demonstrated that phospholipids are incorporated into the larval membranes, where interactions with internal signaling cascades are proposed to occur. Second, we identified two structurally distinct exopolysaccharides of bacterial biofilms, the new Rha-Man polysaccharide from Pseudoalteromonas sp. strain P1-9 and curdlan from Alcaligenes faecalis, to induce metamorphosis in up to 75% of tested larvae. We also found that combinations of (lyso)phospholipids and curdlan induced transformation within 24 h, thereby exceeding the morphogenic activity observed for single compounds and bacterial biofilms. Our results demonstrate that two structurally distinct, bacterium-derived metabolites converge to induce high transformation rates of Hydractinia larvae and thus may help ensure optimal habitat selection. IMPORTANCE Bacterial biofilms profoundly influence the recruitment and settlement of marine invertebrates, critical steps for diverse marine processes such as the formation of coral reefs, the maintenance of marine fisheries, and the fouling of submerged surfaces. However, the complex composition of biofilms often makes the characterization of individual signals and regulatory mechanisms challenging. Developing tractable model systems to characterize these coevolved interactions is the key to understanding fundamental processes in evolutionary biology. Here, we characterized two types of bacterial signaling molecules, phospholipids and polysaccharides, that induce the morphogenic transition. We then analyzed their abundance and combinatorial activity. This study highlights the general importance of multiple bacterial signal converging activity in development-related cross-kingdom signaling and poses the question of whether complex lipids and polysaccharides are general metamorphic cues for cnidarian larvae.

Report on hydrozoans (Cnidaria), excluding Stylasteridae, from the Emperor Seamounts, western North Pacific Ocean.

Fourteen species of hydroids, collected during August 2019 by ROV SuBastian of the Schmidt Ocean Institute, are reported from the Emperor Seamount chain in the western North Pacific Ocean. Two others, Candelabrum sp. and Eudendrium sp., were observed only on videos taken by the ROV. From collections and video observations, eight species of hydroids were found at Jingu Seamount, three at Yomei, Nintoku, and Annei seamounts, and one at Koko Seamount and Hess Rise. At Suiko and Godaigo seamounts, hydroids were seen in videos but they could not be identified. Latebrahydra schulzei, an endobiotic associate of the hexactinellid sponge Walteria flemmingii Schulze, 1886 from Annei Seamount and Hess Rise, is described as a new genus and species tentatively attributed to Hydractiniidae L. Agassiz, 1862. Another new species, Hydractinia galeai, is described from Jingu Seamount. Among its distinctive characters is a zooid termed a sellectozooid, likely serving in both food capture and defence. Hydroids examined from Yomei, Nintoku, and Jingu seamounts are elements of a cold-water fauna occurring in the North Pacific Boreal Bathyal province, while those of Annei and Koko seamounts, and Hess Rise, are part of the biota of the Central North Pacific Bathyal province. Hydroids identified as Bouillonia sp., from Nintoku Seamount, represent the first record of this predominantly deep water tubulariid genus in the North Pacific Ocean. Bonneviella superba Nutting, 1915, from Jingu Seamount, is reported for the first time outside the Aleutian Islands. Bonneviella cf. gracilis Fraser, 1939, known elsewhere only from Dease Strait in the western Canadian Arctic, was also collected on Jingu. In addition to hydroids, medusae of Ptychogastria polaris Allman, 1878 were observed on videos from Nintoku, Jingu, Annei, and Koko seamounts at depths between 2423-1422 m. An unidentified siphonophore was observed near bottom at 2282 m on Nintoku Seamount.

The evolution of siphonophore tentilla for specialized prey capture in the open ocean.

Predator specialization has often been considered an evolutionary "dead end" due to the constraints associated with the evolution of morphological and functional optimizations throughout the organism. However, in some predators, these changes are localized in separate structures dedicated to prey capture. One of the most extreme cases of this modularity can be observed in siphonophores, a clade of pelagic colonial cnidarians that use tentilla (tentacle side branches armed with nematocysts) exclusively for prey capture. Here we study how siphonophore specialists and generalists evolve, and what morphological changes are associated with these transitions. To answer these questions, we: a) Measured 29 morphological characters of tentacles from 45 siphonophore species, b) mapped these data to a phylogenetic tree, and c) analyzed the evolutionary associations between morphological characters and prey-type data from the literature. Instead of a dead end, we found that siphonophore specialists can evolve into generalists, and that specialists on one prey type have directly evolved into specialists on other prey types. Our results show that siphonophore tentillum morphology has strong evolutionary associations with prey type, and suggest that shifts between prey types are linked to shifts in the morphology, mode of evolution, and evolutionary correlations of tentilla and their nematocysts. The evolutionary history of siphonophore specialization helps build a broader perspective on predatory niche diversification via morphological innovation and evolution. These findings contribute to understanding how specialization and morphological evolution have shaped present-day food webs.

Assessment of serpulid-hydroid association through the Jurassic: A case study from the Polish Basin.

The coexistence of sessile, tube-dwelling polychaetes (serpulids) and hydroids, has been investigated. Serpulid tubes bearing traces after hydroids are derived from different stratigraphic intervals spanning the Middle and Upper Jurassic, the rocks of which represent the diverse paleoenvironments of the Polish Basin. Although fossil colonial hydroids classified under the species Protulophila gestroi are a commonly occurring symbiont of these polychaetes during the Late Cretaceous and Cenozoic, they seem to be significantly less frequent during the Jurassic and limited to specific paleoenvironments. The hydroids described here are represented by traces after a thin stolonal network with elongated polyp chambers that open to the outer polychaete tube's surface with small, more or less subcircular apertures. Small chimney-like bulges around openings are an effect of the incorporation of the organism by in vivo embedment (bioclaustration) within the outer layers of the calcareous tube of the serpulid host. Considering the rich collection of well-preserved serpulid tubes (>3000 specimens), the frequency of bioclaustrated hydroids is very low, with an infestation percentage of only 0.6% (20 cases). It has been noticed that only specimens of the genus Propomatoceros from the Upper Bajocian, Lower Bathonian, Middle Bathonian, and Callovian have been found infested. However, the majority of bioclaustrated hydroids (17 cases) have been recorded in the Middle Bathonian serpulid species Propomatoceros lumbricalis coming from a single sampled site. Representatives of other genera are not affected, which is congruent with previous reports indicating that Protulophila gestroi was strongly selective in the choice of its host. A presumably commensal relationship is compared with the recent symbiosis between the hydroids of the genus Proboscidactyla and certain genera of sabellid polychaetes.

Pattern regulation in a regenerating jellyfish.

Jellyfish, with their tetraradial symmetry, offer a novel paradigm for addressing patterning mechanisms during regeneration. Here we show that an interplay between mechanical forces, cell migration and proliferation allows jellyfish fragments to regain shape and functionality rapidly, notably by efficient restoration of the central feeding organ (manubrium). Fragmentation first triggers actomyosin-powered remodeling that restores body umbrella shape, causing radial smooth muscle fibers to converge around 'hubs' which serve as positional landmarks. Stabilization of these hubs, and associated expression of Wnt6, depends on the configuration of the adjoining muscle fiber 'spokes'. Stabilized hubs presage the site of the manubrium blastema, whose growth is Wnt/ß-catenin dependent and fueled by both cell proliferation and long-range cell recruitment. Manubrium morphogenesis is modulated by its connections with the gastrovascular canal system. We conclude that body patterning in regenerating jellyfish emerges mainly from local interactions, triggered and directed by the remodeling process.

Frizzled3 expression and colony development in hydractiniid hydrozoans.

Hydractiniid hydrozoan colonies are comprised of individual polyps connected by tube-like stolons or a sheet-like mat. Mat and stolons function to integrate the colony through continuous epithelia and shared gastrovascular cavity. Although mechanisms of hydrozoan polyp development have been well studied, little is known about the signaling processes governing the patterning of colonies. Here we investigate the Wnt receptor family Frizzled. Phylogenetic analysis reveals that hydrozoans possess four Frizzled orthologs. We find that one of these genes, Frizzled3, shows a spatially restricted expression pattern in colony-specific tissue in two hydractiniid hydrozoans, Hydractinia symbiolongicarpus and Podocoryna carnea, in a manner that corresponds to their distinct colony forms (stolonal mat in Hydractinia and free stolons in Podocoryna). Interestingly, Frizzled3 was lost in the genome of Hydra, which is a solitary polyp and thus lacks colony-specific tissue. Current evidence suggests that the Wnt signaling pathway plays a key role in the evolution of colony diversity and colony loss in Hydrozoa.

Isolation and Characterization of Feeding-Deficient Strains in Inbred Lines of the Hydrozoan Jellyfish Cladonema pacificum.

Feeding behavior in cnidarians has been studied as a model experimental system in physiology and neurobiology. Although the feeding response in cnidarians, such as Hydra, is triggered by chemical signals, the underlying molecular mechanisms that ensure their precise execution are not well understood. It could be largely due to the lack of genetic analysis in cnidarian experimental systems. Cladonema pacificum is a hydrozoan jellyfish that is easy to maintain and cross for genetic analysis in the laboratory. To establish C. pacificum as a model experimental animal in cnidarians, we have been inbreeding strains of jellyfish. Here, we document our progress in developing C. pacificum inbred lines and feeding-defective strains that we isolated in the course of inbreeding. In the inbred lines, an increasing number of feeding-defective strains appeared as descending generations and finally all the F5 progeny showed a feeding-deficient phenotype presumably owing to inbreeding depression. Feeding behaviors of these strains were analyzed by video microscopy and we found that the feeding-defective strains captured prey, but could not kill them. After trapping prey, wild-type medusae contracted their tentacles tightly and then bent the tentacles to bring the prey to the mouth; however, feeding-defective medusae rarely contracted their tentacles and did not bend. These feeding-defective phenotypes are caused by lack of stinging nematocytes in their tentacle batteries. These findings furnish a clue to the regulatory aspects of feeding behavior, but also reveal the mechanisms of stinging nematocyte transport in tentacles.

A G protein-coupled receptor mediates neuropeptide-induced oocyte maturation in the jellyfish Clytia.

The reproductive hormones that trigger oocyte meiotic maturation and release from the ovary vary greatly between animal species. Identification of receptors for these maturation-inducing hormones (MIHs) and understanding how they initiate the largely conserved maturation process remain important challenges. In hydrozoan cnidarians including the jellyfish Clytia hemisphaerica, MIH comprises neuropeptides released from somatic cells of the gonad. We identified the receptor (MIHR) for these MIH neuropeptides in Clytia using cell culture-based "deorphanization" of candidate oocyte-expressed G protein-coupled receptors (GPCRs). MIHR mutant jellyfish generated using CRISPR-Cas9 editing had severe defects in gamete development or in spawning both in males and females. Female gonads, or oocytes isolated from MIHR mutants, failed to respond to synthetic MIH. Treatment with the cAMP analogue Br-cAMP to mimic cAMP rise at maturation onset rescued meiotic maturation and spawning. Injection of inhibitory antibodies to the alpha subunit of the Gs heterodimeric protein (GαS) into wild-type oocytes phenocopied the MIHR mutants. These results provide the molecular links between MIH stimulation and meiotic maturation initiation in hydrozoan oocytes. Molecular phylogeny grouped Clytia MIHR with a subset of bilaterian neuropeptide receptors, including neuropeptide Y, gonadotropin inhibitory hormone (GnIH), pyroglutamylated RFamide, and luqin, all upstream regulators of sexual reproduction. This identification and functional characterization of a cnidarian peptide GPCR advances our understanding of oocyte maturation initiation and sheds light on the evolution of neuropeptide-hormone systems.

A case of nascent speciation: unique polymorphism of gonophores within hydrozoan Sarsia lovenii.

Revealing the mechanisms of life cycle changes is critical for understanding the processes driving hydrozoan evolution. Our analysis of mitochondrial (COI, 16S) and nuclear (ITS1 and ITS2) gene fragments resulted in the discovery of unique polymorphism in the life cycle of Sarsia lovenii from the White Sea. This polymorphic species exhibits two types of gonophores: hydroids produce both free-swimming medusae and attached medusoids (phenotypic polymorphism). Our phylogenetic analysis revealed the intrinsic genetic structure of S. lovenii (genetic polymorphism). Two haplogroups inhabiting the White Sea differ in their reproductive modes. Haplogroup 1 produces attached medusoids, and haplogroup 2 produces free-swimming medusae. Our experiments indicated the possibility of free interbreeding between haplogroups that likely is a rare event in the sea. We propose that inter-haplogroup crossing of S. lovenii in the White Sea may be limited by discordance in periods of spawning or by spatial differences in habitat of spawning specimens. Our finding can be interpreted as a case of nascent speciation that illustrates the patterns of repeated medusa loss in hydrozoan evolution. Life cycle traits of S. lovenii may be useful for elucidating the molecular mechanisms of medusa reduction in hydrozoans.

Macroscale abundance patterns of hydromedusae in the temperate Southwestern Atlantic (27°-56° S).

Gelatinous organisms are crucial components of marine ecosystems and some species imply social and economic consequences. However, certain geographic areas, such as the temperate Southwestern Atlantic (SWA, 27° - 56° S), remain understudied in terms of jellyfish ecological data. We analyzed 3,727 plankton samples collected along ~6.7 million km2 over a 31-year period (1983-2014) to determine the occurrence, abundance, and diversity patterns of hydromedusae in the SWA. Analyses were made at both community and species levels. Two abundance hot spots of hydromedusae were identified, where values up to 2,480 ind. m-3 were recorded between 2003 and 2014. Liriope tetraphylla and Obelia spp. were the main responsible for recurrent peaks. Diversity indexes were in the range of those published for temperate areas worldwide, and some coastal zones showed values that can be considered moderate to high for a temperate neritic region. The community analysis yielded 10 groups following previously determined biogeographic schemes throughout the study area. This work enhances the knowledge of hydromedusae in the SWA and provides essential information about the current global warming context and the gelatinous zooplankton data necessity.

Propulsive design principles in a multi-jet siphonophore.

Coordination of multiple propulsors can provide performance benefits in swimming organisms. Siphonophores are marine colonial organisms that orchestrate the motion of multiple swimming zooids for effective swimming. However, the kinematics at the level of individual swimming zooids (nectophores) have not been examined in detail. We used high-speed, high-resolution microvideography and particle image velocimetry of the physonect siphonophore Nanomia bijuga to study the motion of the nectophores and the associated fluid motion during jetting and refilling. The integration of nectophore and velum kinematics allow for a high-speed (maximum ∼1 m s-1), narrow (1-2 mm) jet and rapid refill, as well as a 1:1 ratio of jetting to refill time. Scaled to the 3 mm nectophore length, jet speeds reach >300 lengths s-1 Overall swimming performance is enhanced by velocity gradients produced in the nectophore during refill, which lead to a high-pressure region that produces forward thrust. Generating thrust during both the jet and refill phases augments the distance traveled by 17% over theoretical animals, which generate thrust only during the jet phase. The details of velum kinematics and associated fluid mechanics elucidate how siphonophores effectively navigate three-dimensional space, and could be applied to exit flow parameters in multijet underwater vehicles.

Phenotypic Plasticity in Animals Exposed to Osmotic Stress - Is it Always Adaptive?

Hyperplasia and hypertrophy are elements of phenotypic plasticity adjusting organ size and function. Because they are costly, we assume that they are beneficial. In this review, the authors discuss examples of tissue and organ systems that respond with plastic changes to osmotic stress to raise awareness that we do not always have sufficient experimental evidence to conclude that such processes provide fitness advantages. Changes in hydranth architecture in the hydroid Cordylophora caspia or variations in size in the anal papillae of insect larvae upon changes in medium salinity may be adaptive or not. The restructuring of salt glands in ducklings upon salt-loading is an example of phenotypic plasticity which indeed seems beneficial. As the genomes of model species are recently sequenced and the animals are easy to rear, these species are suitable study objects to investigate the biological significance of phenotypic plasticity and to study potential epigenetic and other mechanisms underlying phenotypic changes.

Organic contamination as a driver of structural changes of hydroid's assemblages of the coral reefs near to Havana Harbour, Cuba.

Hydroid assemblage's responses to organic contamination were evaluated using sedimentary sterols as explanatory variables. At seven coral reef sites in the Havana west coast, hydroids were collected along three 10 m × 1 m, 10 m deep transects. Five sterols were analysed, i.e., coprostanol, an indicator of faecal contamination, and cholestanol, cholesterol, stigmasterol and brassicasterol, indicators of biogenic organic matter inputs. The sampling sites were classified by level of contamination. A total of 65 species comprised the hydroid assemblages. Hydroids community abundance and richness decreased in the contaminated sites. Coprostanol had the highest relative importance for these variables and also for Plumularia floridana and Clytia gracilis abundances. Obelia dichotoma and Halecium bermudense were relatively abundant in the contaminated sites. The results indicate that faecal contamination negatively affected the hydroid assemblages, highlighting the importance of integrated biological and chemical indicators to evaluate the environmental conditions of the Havana coral reef.

Successional dynamics of marine fouling hydroids (Cnidaria: Hydrozoa) at a finfish aquaculture facility in the Mediterranean Sea.

Aquaculture is increasing rapidly to meet global seafood demand. Some hydroid populations have been linked to mortality and health issues in finfish and shellfish, but their dynamics in and around aquaculture farms remain understudied. In the present work, two experiments, each with 36 panels, tested colonization (factors: depth, season of immersion) and succession (factors: depth, submersion duration) over one year. Hydroid surface cover was estimated for each species, and data were analyzed with multivariate techniques. The assemblage of hydrozoans was species-poor, although species richness, frequency and abundance increased with time, paralleling the overall increase in structural complexity of fouling assemblages. Submersion duration and season of immersion were particularly important in determining the species composition of the assemblages in the succession and colonization experiments, respectively. Production of water-borne propagules, including medusae, from the hydroids was observed from locally abundant colonies, among them the well-known fouling species Obelia dichotoma, potentially representing a nuisance for cultured fish through contact-driven envenomations and gill disorders. The results illustrate the potential importance of fouling hydroids and their medusae to the health of organisms in the aquaculture industry.

A gonad-expressed opsin mediates light-induced spawning in the jellyfish Clytia.

Across the animal kingdom, environmental light cues are widely involved in regulating gamete release, but the molecular and cellular bases of the photoresponsive mechanisms are poorly understood. In hydrozoan jellyfish, spawning is triggered by dark-light or light-dark transitions acting on the gonad, and is mediated by oocyte maturation-inducing neuropeptide hormones (MIHs) released from the ectoderm. We determined in Clytia hemisphaerica that blue-cyan light triggers spawning in isolated gonads. A candidate opsin (Opsin9) was found co-expressed with MIH within specialised ectodermal cells. Opsin9 knockout jellyfish generated by CRISPR/Cas9 failed to undergo oocyte maturation and spawning, a phenotype reversible by synthetic MIH. Gamete maturation and release in Clytia is thus regulated by gonadal photosensory-neurosecretory cells that secrete MIH in response to light via Opsin9. Similar cells in ancestral eumetazoans may have allowed tissue-level photo-regulation of diverse behaviours, a feature elaborated in cnidarians in parallel with expansion of the opsin gene family.

Identification of jellyfish neuropeptides that act directly as oocyte maturation-inducing hormones.

Oocyte meiotic maturation is crucial for sexually reproducing animals, and its core cytoplasmic regulators are highly conserved between species. By contrast, the few known maturation-inducing hormones (MIHs) that act on oocytes to initiate this process are highly variable in their molecular nature. Using the hydrozoan jellyfish species Clytia and Cladonema, which undergo oocyte maturation in response to dark-light and light-dark transitions, respectively, we deduced amidated tetrapeptide sequences from gonad transcriptome data and found that synthetic peptides could induce maturation of isolated oocytes at nanomolar concentrations. Antibody preabsorption experiments conclusively demonstrated that these W/RPRPamide-related neuropeptides account for endogenous MIH activity produced by isolated gonads. We show that the MIH peptides are synthesised by neural-type cells in the gonad, are released following dark-light/light-dark transitions, and probably act on the oocyte surface. They are produced by male as well as female jellyfish and can trigger both sperm and egg release, suggesting a role in spawning coordination. We propose an evolutionary link between hydrozoan MIHs and the neuropeptide hormones that regulate reproduction upstream of MIHs in bilaterian species.

Widespread utilization of passive energy recapture in swimming medusae.

Recently, it has been shown that some medusae are capable of swimming very efficiently, i.e. with a low cost of transport, and that this is in part due to passive energy recapture (PER) which occurs during bell relaxation. We compared the swimming kinematics among a diverse array of medusae, varying in taxonomy, morphology and propulsive and foraging modes, in order to evaluate the prevalence of PER in medusae. We found that while PER was common among taxa, the magnitude of the contribution to overall swimming varied greatly. The ability of medusae to utilize PER was not related to morphology and swimming performance but was controlled by their swimming kinematics. Utilizing PER required the medusae to pause after bell expansion and individuals could modulate their PER by changing their pause duration. PER can greatly enhance swimming efficiency but there appear to be trade-offs associated with utilizing PER.

Corals hosting symbiotic hydrozoans are less susceptible to predation and disease.

In spite of growing evidence that climate change may dramatically affect networks of interacting species, whether-and to what extent-ecological interactions can mediate species' responses to disturbances is an open question. Here we show how a largely overseen association such as that between hydrozoans and scleractinian corals could be possibly associated with a reduction in coral susceptibility to ever-increasing predator and disease outbreaks. We examined 2455 scleractinian colonies (from both Maldivian and the Saudi Arabian coral reefs) searching for non-random patterns in the occurrence of hydrozoans on corals showing signs of different health conditions (i.e. bleaching, algal overgrowth, corallivory and different coral diseases). We show that, after accounting for geographical, ecological and co-evolutionary factors, signs of disease and corallivory are significantly lower in coral colonies hosting hydrozoans than in hydrozoan-free ones. This finding has important implications for our understanding of the ecology of coral reefs, and for their conservation in the current scenario of global change, because it suggests that symbiotic hydrozoans may play an active role in protecting their scleractinian hosts from stresses induced by warming water temperatures.

Kleptopredation: a mechanism to facilitate planktivory in a benthic mollusc.

Predation occurs when an organism completely or partially consumes its prey. Partial consumption is typical of herbivores but is also common in some marine microbenthic carnivores that feed on colonial organisms. Associations between nudibranch molluscs and colonial hydroids have long been assumed to be simple predator-prey relationships. Here we show that while the aeolid nudibranch Cratena peregrina does prey directly on the hydranths of Eudendrium racemosum, it is stimulated to feed when hydranths have captured and are handling prey, thus ingesting recently captured plankton along with the hydroid polyp such that plankton form at least half of the nudibranch diet. The nudibranch is thus largely planktivorous, facilitated by use of the hydroid for prey capture. At the scale of the colony this combines predation with kleptoparasitism, a type of competition that involves the theft of already-procured items to form a feeding mode that does not fit into existing classifications, which we term kleptopredation. This strategy of subsidized predation helps explain how obligate-feeding nudibranchs obtain sufficient energy for reproduction from an ephemeral food source.