Biology subjects

Costello, J. H.

Publications and source records attributed to Costello, J. H..

9 recordsLinked to original sources

bioRxiv2024

Impactful feeding ecology of a predatory guild of oceanic jellies

Planktonic organisms are integral members of open ocean ecosystems and are critical drivers of material cycles in the worlds oceans. Ctenophores may be numerically dominant predators in these oceanic ecosystems but have been ignored due to the difficulty in both sampling and handling their extremely delicate, gelatinous bodies. To better understand their trophic impact, we combined SCUBA with novel imaging techniques to non-invasively document prey ingestion patterns of four widespread oceanic ctenophore species. We found that these ctenophores ingested 32 prey per hour and the most voracious species ingested nearly 50 prey per hour. Further, the size and number of prey ingested increased with ctenophore size. At these rates, lobate and cestid ctenophores consume prey at similar rates to their highly impactful coastal relative, Mnemiopsis leidyi and are likely the most impactful planktonic predator in the open oceans. Further, we showed that although major dietary components overlapped, different oceanic ctenophore species appear to specialize on different members of the plankton. Since these oceanic ctenophore species frequently co-occur, they comprise a powerful guild of influential planktonic predators with synergistic impacts. These results indicate that epipelagic ctenophores have much greater trophic effects on material cycles over broad areas of the open ocean than previously considered. Models of oceanic carbon cycling will benefit by more fully incorporating the impacts of oceanic ctenophores on their planktonic prey.

ecology↗

bioRxiv2024

Colonial Architecture Modulates the Speed and Efficiency of Multi-Jet Swimming in Salp Colonies

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. We hypothesize that colonial architecture drives differences in swimming performance between salps due to differences in how frontal drag scales with the number of propeller zooids in the colony. Moreover, we hypothesize that faster-swimming taxa are more energetically efficient in their locomotion since less energy would be devoted to overcoming drag forces. We (1) compare swimming speed across salp species and architectures, (2) evaluate how swimming speed scales with the number of zooids in the colony in architectures with constant and scaling frontal cross-sectional area, and (3) compare the metabolic cost of transport across different species and how it scales with swimming speed. To measure their 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 generally swim faster and with a lower cost of transport due to their differential advantage in frontal drag scaling with an increasing number of zooids. 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. Summary StatementLinear arrangements in multi-jet propelled marine colonial invertebrates are faster and more energetically efficient than less streamlined architectures, offering insights for bioinspired underwater vehicle design.

zoology↗

bioRxiv2023

Nectophore coordination and kinematics by physonect siphonophores

Siphonophores are ubiquitous and often highly abundant members of pelagic ecosystems throughout the open ocean. They are unique among animal taxa in that they use multiple jets for propulsion. Little is known about kinematics of the individual jets produced by nectophores or how the jets are coordinated during normal swimming behavior. Using remotely operated vehicles and SCUBA, we video recorded the swimming behavior of several physonect species in their natural environment. The pulsed kinematics of the individual nectophores that comprise the siphonophore nectosome were quantified and, based on these kinematics, we examined the coordination of adjacent nectophores. We found for all species that nectophores sharing the same side of the nectosomal axis were coordinated metachronally. However, this coordination was not shared with nectophores on the opposite side of the nectosomal axis. For most species, the metachronal contraction waves of nectophores were initiated by the apical nectophores and traveled dorsally. However, the metachronal wave of Apolemia rubriversa traveled in the opposite direction. Although nectophore groups on opposite sides of the nectosome were not coordinated, they pulsed with similar frequencies. This enabled siphonophores to maintain relatively linear trajectories during swimming. The timing and characteristics of the metachronal coordination of pulsed jets affects how the jet wakes interact and may provide important insight into how interacting jets may be optimized for efficient propulsion.

zoology↗

bioRxiv2023

Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor

Evolution of multicellularity from early unicellular ancestors is arguably one of the most important transitions since the origin of life1,2. Multicellularity is often associated with higher nutrient uptake3, better defense against predation, cell specialization and better division of labor4. While many single-celled organisms exhibit both solitary and colonial existence3,5,6, the organizing principles governing the transition and the benefits endowed are less clear. Using the suspension-feeding unicellular protist Stentor coeruleus, we show that hydrodynamic coupling between proximal neighbors results in faster feeding flows that depend on the separation between individuals. Moreover, we find that the accrued benefits in feeding current enhancement are typically asymmetric- individuals with slower solitary currents gain more from partnering than those with faster currents. We find that colony-formation is ephemeral in Stentor and individuals in colonies are highly dynamic unlike other colony-forming organisms like Volvox carteri 3. Our results demonstrate benefits endowed by the colonial organization in a simple unicellular organism and can potentially provide fundamental insights into the selective forces favoring early evolution of multicellular organization.

biophysics↗

bioRxiv2021

Swimming kinematics and performance of spinal transected lampreys with different levels of axon regeneration

Neural and functional recovery in lampreys from spinal cord transection has been well documented. However, the extent of axon regeneration is highly variable and it is not known whether it is related to the level of behavioral recovery. To address this, we examined how swimming kinematics were related to axon regeneration by quantifying the relationship between swimming performance and percent axon regeneration of transected lampreys after 11 weeks of recovery. We found that swimming speed was not related to percent axon regeneration but it was closely related to body wave frequency and speed. However, wave frequency and speed varied greatly within individuals which resulted in swimming speed also varying within individuals. In fact, most recovered individuals, regardless of percent axon regeneration, could swim at fast and slow speeds. However, none of the transected individuals were able to generate body waves as large as the control lampreys. In order to swim faster, transected lampreys increased their wave frequencies and, as a result, transected lampreys had much higher frequencies than control lamprey at comparable swimming velocities. These data suggest that the control lampreys swam more efficiently than transected lampreys. In conclusion, there appears to be a minimal recovery threshold in terms of percent axon regeneration required for lampreys to be capable of swimming, however, there also seems to be a limit to how much they can behaviorally recover.

animal behavior and cognition↗

bioRxiv2020

The most efficient metazoan swimmer creates a 'virtual wall' to enhance performance

It has been well documented that animals (and machines) swimming or flying near a solid boundary get a boost in performance1-6. This ground effect is often modeled as an interaction between a mirrored pair of vortices represented by a true vortex and an opposite sign virtual vortex on the other side of the wall7. However, most animals do not swim near solid surfaces and thus near body vortex-vortex interactions in open-water swimmers have been poorly investigated. In this study we examine the most energetically efficient metazoan swimmer known to date, the jellyfish Aurelia aurita, to elucidate the role that vortex interactions can play in animals that swim away from solid boundaries. We used high speed video tracking, laser-based digital particle image velocimetry (dPIV) and an algorithm for extracting pressure fields from flow velocity vectors to quantify swimming performance and the effect of near body vortex-vortex interactions. Here we show that a vortex ring (stopping vortex), created underneath the animal during the previous swim cycle, is critical for increasing propulsive performance. This well positioned stopping vortex acts in the same way as a virtual vortex during wall-effect performance enhancement, by helping converge fluid at the underside of the propulsive surface and generating significantly higher pressures which result in greater thrust. These findings advocate that jellyfish can generate a wall-effect boost in open water by creating what amounts to a virtual wall between two real, opposite sign vortex rings. This explains the significant propulsive advantage jellyfish possess over other metazoans and represents important implications for bio-engineered propulsion systems.

animal behavior and cognition↗

bioRxiv2019

Primitive and modern swimmers solve the challenges of turning similarly to achieve high maneuverability

Animal swimmers alter trajectories - or turn - for a variety of critical life functions such as feeding, mating and avoiding predation. Yet turning represents a fundamental dilemma based in rotational dynamics: the torque powering a turn is favored by an expanded body configuration, yet minimizing the resistance to a turn (the moment of inertia) is favored by a contracted body configuration. How do animals balance these opposing demands to achieve high maneuverability? By noninvasively measuring fluid and body motions, we found that both jellyfish (Aurelia aurita) and fish (Danio rerio) initially maximized torque using previously undescribed, rapid body movements. Both species then minimized resistance to turning by bending their bodies to reduce their moment of inertia. Use of this sequential solution by such distantly related animals as an invertebrate and a vertebrate suggests strong selection for these turning dynamics that may extend to other swimmers and inform future vehicle designs.

zoology↗

bioRxiv2018

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 (PIV) 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. 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 travelled 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.\n\nSummary statementColonial siphonophores produce high speed jets and generate forward thrust during refill using a flexible velum to achieve effective propulsion.

biophysics↗

bioRxiv2017

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 is commonly observed 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. Passive energy recapture can greatly enhance swimming efficiency but there appear to be trade-offs associated with utilizing PER.

animal behavior and cognition↗