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Thoracian barnacles rely heavily upon their ability to adhere to surfaces and are environmentally and economically important as biofouling pests. Their adhesives have unique attributes that define them as targets for bio-inspired adhesive development. With the aid of multi-photon and broadband coherent anti-Stokes Raman scattering microscopies, we report that the larval adhesive of barnacle cyprids is a bi-phasic system containing lipids and phosphoproteins, working synergistically to maximize adhesion to diverse surfaces under hostile conditions. Lipids, secreted first, possibly displace water from the surface interface creating a conducive environment for introduction of phosphoproteins while simultaneously modulating the spreading of the protein phase and protecting the nascent adhesive plaque from bacterial biodegradation. The two distinct phases are contained within two different granules in the cyprid cement glands, implying far greater complexity than previously recognized. Knowledge of the lipidic contribution will hopefully inspire development of novel synthetic bioadhesives and environmentally benign antifouling coatings. Using their unique bioadhesives, barnacles can adhere to a great variety of surfaces. Here, Gohad et al. show that the barnacle larval bioadhesive contains lipids and phosphoproteins that are organized in a complex structure and work together to maximize adhesion.

The striped barnacle, Amphibalanus amphitrite, is a simultaneous hermaphrodite crustacean that broods eggs. The eggs are physically and enzymatically cleaned in the mantle by the barnacle to manage biofouling during incubation. There is no physiological connection between the embryos and the adult. Instead, barnacles use enzyme products as pheromones to coordinate behavioral, physiological, and biochemical processes involved in egg hatching and larval release. Known larval release pheromones are peptides generated by exogenous trypsins that act on proteins. We characterized barnacle brooding endoproteinases using a proteomic analysis of peptides generated from the hydrolysis of pure proteins that were identified by high-resolution LC electrospray MS/MS. Utilizing pure proteins permitted us to completely identify sequences around proteolytic cleavage sites. Enzyme activity was 2.22 to 2.79 times greater in barnacle and barnacle microbiome samples compared to seawater samples. Distinct enzyme patterns emerged, with higher proline- and asparagine-cutting enzymes in barnacle samples and greater proportions of elastase in seawater. There are at least 13 endoproteinases based on the C-terminus amino acids of peptides, with major contributions from serine proteases. This approach has the potential to provide exceptionally detailed information on endoproteinases in any microbiome assemblage. With a little thought, this technique can be expanded to include exoproteinases as well.

Although mathematical models and laboratory experiments have shown that species interactions can generate chaos, field evidence of chaos in natural ecosystems is rare. We report on a pristine rocky intertidal community located in one of the world’s oldest marine reserves that has displayed a complex cyclic succession for more than 20 y. Bare rock was colonized by barnacles and crustose algae, they were overgrown by mussels, and the subsequent detachment of the mussels returned bare rock again. These processes generated irregular species fluctuations, such that the species coexisted over many generations without ever approaching a stable equilibrium state. Analysis of the species fluctuations revealed a dominant periodicity of about 2 y, a global Lyapunov exponent statistically indistinguishable from zero, and local Lyapunov exponents that alternated systematically between negative and positive values. This pattern indicates that the community moved back and forth between stabilizing and chaotic dynamics during the cyclic succession. The results are supported by a patch-occupancy model predicting similar patterns when the species interactions were exposed to seasonal variation. Our findings show that natural ecosystems can sustain continued changes in species abundances and that seasonal forcing may push these nonequilibrium dynamics to the edge of chaos. Significance The intuitive and popular idea of a balance of nature has been criticized, because species interactions may generate nonequilibrium dynamics, such as oscillations and chaos. However, field evidence of chaos in ecosystems is rare. We report on a coastal community that has displayed striking fluctuations in the abundances of barnacles, mussels, and algae for more than 20 y. Data analysis reveals that these fluctuations reflect a cyclic succession alternating between stabilizing and chaotic dynamics during the species replacement. These results are supported by a simple patch-occupancy model, which predicts very similar dynamics when exposed to seasonal variation. Our findings provide a field demonstration of nonequilibrium coexistence of competing species through a cyclic succession at the edge of chaos.

Coastal regions support approximately 60% of the global population and face escalating anthropogenic pollution, which disrupts the dynamics of marine and coastal ecosystems. The discharge of over 80% of sewage without adequate treatment introduces human pathogenic microorganisms into coastal waters, posing significant risks to ecological integrity and public health. This challenge is exacerbated by cross‐resistance between antibiotics and biocides, whereby biocide use for biofilm control in coastal industries may inadvertently select for resistant pathogens of terrestrial origin. While microbial biofilms are known to promote macrofouling by facilitating invertebrate larval settlement, a major operational challenge for marine industries, the role of anthropogenic microbial contamination in influencing macrofouling dynamics remains poorly understood. Here, we provide evidence linking anthropogenic microbial contamination to marine biofouling. We isolated an antibiotic and biocide‐resistant Enterobacter cloacae strain from a marine cooling water circuit at an operational power plant and identified it as a potent inducer of barnacle (Amphibalanus reticulatus) larval settlement. Salt‐tolerance assays combined with Multi‐Locus Sequence Typing (MLST) and AAI/ANI‐based comparative genomics against reference strains indicated a likely terrestrial origin for this isolate. Larval settlement and choice assays demonstrated that E. cloacae biofilms increased barnacle settlement by > 70% relative to controls. To develop sustainable mitigation strategies against this biocide‐resistant organism, we isolated natural bacteriophages targeting E. cloacae from the same water sample. Phage‐mediated selective elimination of E. cloacae from biofilms reduced larval settlement by 80% in plate‐based assays, providing proof of concept for bacteriophage‐based targeted elimination of biofouling‐promoting bacteria. Our findings reveal a previously unrecognised connection between anthropogenic bacterial contamination and biofouling dynamics, establishing bacteriophages as an environmentally sustainable strategy for controlling biofilm‐mediated larval settlement in marine industries. Anthropogenic‐derived E. cloacae colonises marine cooling water systems, where chlorine exposure drives cross‐resistance and enhances biofilm formation, creating hotspots for barnacle larval settlement. This work reveals a previously unrecognised mechanism linking microbial pollution to marine biofouling. A native bacteriophage isolated from the same system effectively disrupts these resistant biofilms and reduces larval settlement, offering a sustainable biofouling control strategy.

Water molecules pose a significant obstacle to conventional adhesive materials. Nevertheless, some marine organisms can secrete bioadhesives with remarkable adhesion properties. For instance, mussels resist sea waves using byssal threads, sandcastle worms secrete sandcastle glue to construct shelters, and barnacles adhere to various surfaces using their barnacle cement. This work initially elucidates the process of underwater adhesion and the microstructure of bioadhesives in these three exemplary marine organisms. The formation of bioadhesive microstructures is intimately related to the aquatic environment. Subsequently, the adhesion mechanisms employed by mussel byssal threads, sandcastle glue, and barnacle cement are demonstrated at the molecular level. The comprehension of adhesion mechanisms has promoted various biomimetic adhesive systems: DOPA-based biomimetic adhesives inspired by the chemical composition of mussel byssal proteins; polyelectrolyte hydrogels enlightened by sandcastle glue and phase transitions; and novel biomimetic adhesives derived from the multiple interactions and nanofiber-like structures within barnacle cement. Underwater biomimetic adhesion continues to encounter multifaceted challenges despite notable advancements. Hence, this work examines the current challenges confronting underwater biomimetic adhesion in the last part, which provides novel perspectives and directions for future research.

Most intertidal invertebrates align feeding and reproduction with the tidal cycle. However, it is unknown to what extent biological clocks are involved in these activities. We focused on the internal and external regulation of cirral activity in Fistulobalanus albicostatus , an intertidal barnacle. Barnacles were subjected to a light–dark cycle (LD) for 14 days, constant darkness (DD) for 14 days, or constant light (LL) for 13 days, while monitoring the changes in cirral activity under laboratory conditions. LD individuals showed a major peak in activity repeating in 24 h, while DD and LL caused two peaks per day repeating at approximately 12 h. The 24 h day-active or day-inactive rhythm under LD often disappeared or showed no clear circadian component after transition to DD. Rayleigh’s test showed that activity onset was significantly clustered around specific tidal phases in most experiments, indicating a stable phase-locked circatidal rhythm. Additionally, the timing of collection from the field appeared to influence the response of the cirral activity to the light treatments. These differences in activity may be linked to tidal seasonality. We conclude that F. albicostatus possesses a plastic circatidal rhythm, and that this behavioural flexibility aids adaptation to the demanding intertidal environment.

Background Microhabitat environmental factors (e.g., temperature, oxygen concentration, nutrients, osmotic stress, and topography) are critical to the survival of intertidal organisms. Understanding how transcription responses are regulated in relation to intertidal microhabitat variation has important implications for studying adaptive evolution in these organisms. The barnacle Chthamalus challengeri , which survives in the intertidal zone and is subjected to periodic tidal changes, serves as an ideal species for detecting adaptive evolution in intertidal organisms. Results In this study, we designed a series of in situ tidal conditions for C. challengeri and sequenced their transcriptome collected from various microhabitats. We aimed to detect the genetic adaptation mechanisms of barnacles responding to the microhabitat changes in the intertidal zone based on comparative transcriptomics. Our results indicated that different intertidal microhabitats significantly affected the gene expression models of C. challengeri , particularly for genes related to physiological and biochemical functions. Specifically, the expression of genes such as CYP450, HSP70, CYTB, and COX1 was significantly increased under low tide (air-exposed conditions), while genes like CNGA3, AK, and CP52 showed significantly increased expression under high tide (seawater-immersed conditions). Conclusion The results suggest that C. challengeri relies on cytochrome p450 enzymes to enhance oxidative capacity, counts on heat shock proteins and cell phagocytosis to resist microhabitat changes in response to different tidal conditions, and produces a hypoxic stress response to regulate energy metabolism and body temperature changes upon entering into seawater. This study provides genetic resources and clues for investigating the adaptation mechanisms of intertidal barnacles and identifies different gene expression models for C. challengeri responding to various microhabitats.

Recruitment is a key demographic step for the persistence of populations, so understanding its drivers has traditionally been a relevant goal of ecology. On marine rocky shores, coastal oceanography is an important driver of the recruitment of intertidal invertebrates that reproduce through pelagic larvae by affecting larval transport and delivery. The intermittent upwelling hypothesis (IUH) posits that coastal pelagic larvae are driven offshore under intense upwelling or to depths under intense downwelling, while weak upwelling allows larvae to stay near the shore, thereby facilitating intertidal recruitment. The IUH thus predicts a unimodal relationship between Bakun’s upwelling index (BUI) and intertidal recruitment. The IUH has been supported by studies that plotted simultaneously single average values of recruitment and BUI for various coastal locations that collectively span downwelling to upwelling conditions. Based on its theoretical foundations, the IUH should also hold for a target location analyzed over the years provided enough interannual variation in BUI. On the Atlantic Canadian coast in Nova Scotia, upwelling varies interannually depending on wind patterns. Therefore, for a location that is representative of the abiotic and biotic conditions on this coast (Western Head), we tested the IUH by measuring annual intertidal barnacle recruitment and BUI for the pelagic larval season of barnacles for a period of 10 years (2014–2024). On this coast, BUI averaged for the barnacle larval season varied among years from mild downwelling to clear upwelling. Generalized additive modelling revealed a unimodal relationship between intertidal barnacle recruitment and BUI, thereby supporting the IUH. These results add this western ocean boundary to the known list of coastal systems where upwelling may influence intertidal invertebrate recruitment.

For barnacle cypris larvae at the point of settlement, selection of an appropriate surface is critical. Since post-settlement relocation is usually impossible, barnacles have evolved finely tuned surface-sensing capabilities to identify suitable substrata, and a temporary adhesion system for extensive surface exploration. The pattern of exploratory behaviour appears complex and may last for several hours, imposing significant barriers to quantitative measurement. Here, we employ a novel tracking system that enables simultaneous analysis of the larval body movement of multiple individuals over their entire planktonic phase. For the first time, to our knowledge, we describe quantitatively the complete settlement process of cyprids as they explore and select surfaces for attachment. We confirm the ‘classic’ behaviours of wide searching, close searching and inspection that comprise a model originally proposed by Prof. Dennis Crisp FRS. Moreover, a short-term assay of cyprid body movement has identified inspection behaviour as the best indicator of propensity to settle, with more inspection-related movements occurring in conditions that also promote higher settlement. More than half a century after the model was first proposed by Crisp, there exists a precise method for quantifying cyprid settlement behaviour in wide-ranging investigations of barnacle ecology and applied studies of fouling management.

Rhizocephala, a group of parasitic castrators of other crustaceans, shows remarkable morphological adaptations to their lifestyle. The adult female parasite consists of a body that can be differentiated into two distinct regions: a sac-like structure containing the reproductive organs (the externa), and a trophic, root like system situated inside the hosts body (the interna). Parasitism results in the castration of their hosts, achieved by absorbing the entire reproductive energy of the host. Thus, the ratio of the host and parasite sizes is crucial for the understanding of the parasite’s energetic cost. Using advanced imaging methods (micro-CT in conjunction with 3D modeling), we measured the volume of parasitic structures (externa, interna, egg mass, egg number, visceral mass) and the volume of the entire host. Our results show positive correlations between the volume of (1) entire rhizocephalan (externa + interna) and host body, (2) rhizocephalan externa and host body, (3) rhizocephalan visceral mass and rhizocephalan body, (4) egg mass and rhizocephalan externa, (5) rhizocephalan egg mass and their egg number. Comparing the rhizocephalan Sylon hippolytes, a parasite of caridean shrimps, and representatives of Peltogaster, parasites of hermit crabs, we could match their different traits on a reconstructed relationship. With this study we add new and significant information to our global understanding of the evolution of parasitic castrators, of interactions between a parasitic castrator and its host and of different parasitic strategies within parasitic castrators exemplified by rhizocephalans.