John H. Costello

Summary: The deepest ocean is one of the most extreme environments for life on our planet, combining near-freezing temperatures, low oxygen levels, and hydrostatic pressures reaching 111 MPa (1100 atm). Extreme pressures are predicted to alter many aspects of biology, including the physical properties of biological hydrogels, protein structure, and the solubility of gases in water. How organisms have adapted to live in these conditions is poorly understood. Studying these organisms in situ is difficult and requires specialized deep-sea equipment capable of withstanding the extreme pressure; raising these organisms in captivity is also challenging due to their extreme habitat requirements. Given these difficulties in studying deep-sea organisms, we set out to identify the problems shallow-dwelling organisms face due to increased pressure. These can provide insights into how organisms tolerate life in the deepest parts of the ocean. This project aims to take embryos of the shallow-dwelling aquatic organism Xenopus laevis , determine how surface-dwelling organisms fail under high hydrostatic pressure, and identify a means to survive this deadly pressure. We have designed a system to expose different embryonic stages of X. laevis to high pressures and observe its effects. After identifying the limits of survivability, we sought to understand how these embryos can acclimate to changing pressures. Comparative RNA-seq and cross-species analyses revealed a conserved, pressure-induced transcriptional response across phyla, with the heat shock pathway among the most strongly activated. Pre-activation of this pathway via prior pressure or other stressors enhances survival under otherwise lethal hydrostatic conditions.

Ocean monitoring is essential for understanding climate change and marine ecosystem dynamics, yet achieving comprehensive global coverage remains a challenge in oceanography. Current technologies face limitations in cost, power, hardware, and depth capacity that restrict widespread monitoring capabilities. Here we show that biohybrid robotic jellyfish (Aurelia aurita) can serve as autonomous vertical ocean profilers by integrating microcontrollers with positively buoyant sensor payloads, achieving controlled vertical-profiling capabilities. Laboratory experiments demonstrated repeatable up–down trajectories, quantified force balance limits, and identified predictable, size-dependent descent swimming speeds. Field deployments in Massachusetts coastal waters and the open ocean off the Florida Keys demonstrated field operation to ocean depths >25 m with successful in situ temperature and depth measurements. To our knowledge, this represents the first biohybrid jellyfish platform to combine autonomous, pressure-triggered vertical profiling with onboard oceanographic sensing in natural marine environments. This approach leverages the global distribution and remarkable swimming efficiency of living jellyfish while eliminating propulsion power requirements by utilizing the animal’s natural swimming capabilities. While further development is required for long-term ocean deployment, this study lays the groundwork for a new class of biohybrid ocean-sensing platforms with advantages in cost, power, and mission flexibility, providing a pathway toward dense sensor networks and increased ocean monitoring observations.

Hydromedusae are often overlooked in pelagic trophic ecology compared to large scyphozoans. We investigated the diet, prey selectivity, ingestion rates, digestion times, and predation impacts of the native Liriope tetraphylla and non‐indigenous species Cnidostoma fallax and Moerisia inkermanica in a subtropical estuary of the southwestern Atlantic. While all three species predominantly consumed copepods, L. tetraphylla exhibited the broadest diet and highest number of preys in gut content (up to 13). Digestion time for L. tetraphylla decreased significantly with increasing temperature, from 94 min at 18°C to 64 min at 28°C, with Q ₁₀ values showing that digestion rates roughly double with a 10°C increase. Cnidostoma fallax exhibited longer digestion times (180 min at 23°C). Daily ingestion rations ranged from 16 to 212 copepods day ⁻¹ for L. tetraphylla , 7–15 for C. fallax , and up to 48 for M. inkermanica . Predation impact (PI), the proportion of a prey stock consumed by L. tetraphylla population, averaged 38.1% and peaked at 103.5%, while C. fallax and M. inkermanica had lower impacts (~ 5%). Carbon intake analyses revealed that L. tetraphylla consumed daily up to 280 times its own carbon weight, far exceeding the non‐indigenous species. These results highlight the critical role of hydromedusae in estuarine food webs, challenging the prevailing view that only large gelatinous predators exert top‐down control. We demonstrate that small hydrozoans can be key agents shaping prey community structure and carbon flow in subtropical estuarine ecosystems.

Motility endows microorganisms with the ability to swim to nutrient-rich environments, but many species are sessile. Existing hydrodynamic arguments in support of either strategy, to swim or to attach and generate feeding currents, are often built on a limited set of experimental or modeling assumptions. Here, to assess the hydrodynamics of these ‘swim’ or ‘stay’ strategies, we propose a comprehensive methodology that combines mechanistic modeling with a survey of published shape and flow data in ciliates. Model predictions and empirical observations show small variations in feeding rates in favor of either motile or sessile cells. Case-specific variations notwithstanding, our overarching analysis shows that flow physics imposes no constraint on the feeding rates that are achievable by the swimming versus sessile strategies – they can both be equally competitive in transporting nutrients and wastes to and from the cell surface within flow regimes typically experienced by ciliates. Our findings help resolve a long-standing dilemma of which strategy is hydrodynamically optimal and explain patterns occurring in natural communities that alternate between free swimming and temporary attachments. Importantly, our findings indicate that the evolutionary pressures that shaped these strategies acted in concert with, not against, flow physics.

Hydrostatic pressure in the marine environment increases linearly with depth, and organisms at 1000 m experience pressures 100 times greater than those at sea surface level. Previous work has examined the effects of pressure on neuron and nervous system activity in some organisms, as well as the various biochemical adaptations of deep-water species. However, the effects of pressure on other biological tissues are not well understood. In this study, we took the shallow-water jellyfish Aurelia aurita and exposed it to pressures of up to 30 MPa (equivalent to 3000 m depth). We observed behavioral and kinematic changes that are likely due to mechanical effects of hydrostatic pressure on the swimming muscles and bell mesoglea. The pulsation rate of the bell was found to correlate with hydrostatic pressure, although the effect was small relative to the variability between individuals. Both the maximum contraction and relaxation rates of the bell were found to be significantly reduced at high pressure (30 MPa) relative to near-surface pressure (<1 MPa). The changes in pulse frequency and relaxation rate were both fully and immediately reversed upon release of pressure, but the change to contraction rate was not. Because bell contraction is controlled by muscle fibers and relaxation is controlled by elastic fibers in the mesoglea, the differential effects on contraction versus relaxation suggest that different tissues are affected differently by pressure. This opens the way for future work on how individual organisms can adapt to different environments.

Jellyfish biohybrid robots have been demonstrated to be successfully programmed to perform vertical sampling profiles of the ocean water column. However, the jellyfish’s endogenous swimming behavior can interfere with the controlled swim cycles, decreasing performance. Further, the model animal used to date, Aurelia aurita, is a relatively slow, weakly swimming species. To enhance the performance of the biohybrid vehicles, we tested whether removing the swimming pacemaker of the jellyfish, the rhopalia, eliminated endogenous movements and enhanced responsiveness of the jellyfish to the swim controller. Further, we tested the responsiveness of two fast-swimming jellyfish species, the rhizostome Cassiopea spp. and the cubomedusae Alatina alata. We found in field trials, where the jellyfish swam controlled vertical profiles in the ocean, that removal of rhopalia eliminated all endogenous behaviors and greatly improved the responsiveness of the jellyfish to the swim controller. This was especially true for species with strong endogenous behaviors that prevented the controller from manipulating swim pulses. Further, we found that both Cassiopea spp. and A. alata were highly responsive to the swim controller and that these faster-swimming jellyfish species greatly increased the speed at which the biohybrid vehicle could traverse vertical profiles in the water column. These enhancements greatly increase the reliability and versatility of jellyfish biohybrid robot vehicles.

Phagotrophy, the ability of cells to ingest organic particles, marked a pivotal milestone in evolution, enabling the emergence of single-celled eukaryotes that consume other organisms and leading to multicellular life. However, reliance on food particles also created a mechanical challenge—how to coordinate the transfer of particles from the exterior environment to the cell interior? Here, we investigate this important link using mechanistic models of ciliates, a clade of single-celled eukaryotes that either swim or attach and generate feeding currents to capture prey. We demonstrate that ciliates optimize their feeding efficiency by designating a specific portion of the cell surface as a ‘mouth,’ and optimal cilia coverage varies by life strategy: for sessile ciliates, prey encounter is most efficient when cilia are arranged in bands around oral structures while ciliates that swim display diverse ciliary arrangements that meet the cell’s nutritional needs. Importantly, beyond a threshold of doubling nutrient uptake, further increases in feeding flux do not seem to be a dominant selective force in cell design.

Many single-celled organisms exhibit both solitary and colonial existence. An important step towards multicellularity, which is associated with benefits such as enhanced nutrient uptake, was the formation of colonies of unicellular organisms. However, the initial drivers that favoured individual cells aggregating into more complex colonies are less clear. Here we show that hydrodynamic coupling between proximate neighbours results in faster feeding flows for neighbouring ciliates, such that individuals within a dynamic colony have stronger average feeding flows than solitary individuals. Flows generated by individuals acting together reach higher velocities, thus allowing access to a wider range of prey resources than individuals acting on their own. Moreover, we find that accrued feeding benefits are typically asymmetric: whereas all individuals benefit from acting together, those with slower solitary currents gain more from partnering than those with faster currents. We find that colonial organization in simple unicellular organisms is beneficial for all its members. This provides fundamental insights into the selective forces favouring the early evolution of multicellular organization.

Salps are marine pelagic tunicates with a complex life cycle including a solitary and colonial stage. Salp colonies are composed of asexually budded individuals that coordinate their swimming by multi-jet propulsion. Colonies develop into species-specific architectures with distinct zooid orientations. These distinct colonial architectures vary in how frontal area scales with the number of zooids in the colony. Here, we address how differences in frontal area drive differences in swimming speed and the relationship between swimming speed and cost of transport in salps. We (1) compared swimming speed across salp species and architectures, (2) evaluated how swimming speed scales with the number of zooids across colony in architectures, and (3) compared the metabolic cost of transport across species and how it scales with swimming speed. To measure swimming speeds, we recorded swimming salp colonies using in situ videography while SCUBA diving in the open ocean. To estimate the cost of transport, we measured the respiration rates of swimming and anesthetized salps collected in situ using jars equipped with non-invasive oxygen sensors. We found that linear colonies swim faster, which supports the idea that their differential advantage in frontal area scales with an increasing number of zooids. We also found that higher swimming speeds predict lower costs of transport in salps. These findings underscore the importance of considering propeller arrangement to optimize speed and energy efficiency in bioinspired underwater vehicle design, leveraging lessons learned from the diverse natural laboratory provided by salp diversity.

Understanding the movement patterns and behavior of marine organisms is fundamental for numerous ecological, conservation and management applications. Over the past several decades, advancements in tracking technologies and analytical methods have revolutionized our ability to study marine animal movements. Oceanic zooplankton often make up the bulk of the macroscopic animal biomass in the oceans, yet we know very little about the life histories, migrations and long-term behaviors of these ecologically important animals. In this Review, we consider recent developments in marine movement ecology and animal tracking techniques of gelatinous zooplankton, and discuss the challenges, opportunities and future directions in this rapidly evolving field.