Valentina Di Santo | Stockholm University (original) (raw)
Papers by Valentina Di Santo
We consider the propulsive performance of an unsteady heaving and bending foil with shape inspire... more We consider the propulsive performance of an unsteady heaving and bending foil with shape inspired by Thunniform swimmers such as tuna, computationally studying a parameter space of Strouhal Number and phase offsets between heave and bend motions. The phase offset í µí½ between the heaving and bending motions proves to be critical in determining the propulsive performance and flow structure of the fish-shaped panel. To maximize thrust, the heave and bend motions have to be almost in-phase but not completely (í µí½ ~ 330°), while to maximize efficiency, the bending motion needs to lag the heave motion by about one-fourth of period, which results in a motion of caudal fin at a modest angle of attack, which is similar to biology. I. Nomenclature í µí°´= µí°´= trailing edge amplitude í µí° ¶ í µí°¿ = lift coefficient í µí° ¶ í µí± = thrust coefficient í µí± = foil chord í µí± = foil span í µí±í µí±¡ = time step í µí± = frequency of motion ℎ = leading edge heave position í µí± ∞ = free stream velocity í µí±í µí±¡ = Strouhal number, í µí±í µí±¡ = 2í µí±í µí°´/í µí± ∞ í µí»¼ = angle of attack í µí¼ = propulsive effieciency, í µí¼ = í µí° ¶ í µí± /í µí° ¶ í µí± í µí¼ = pitch angle í µí¼ = kinematic viscosity í µí¼ = fluid density í µí¼ = phase angle between heave and bend motions
We present unifying rules governing the efficient locomotion of swimming fish and marine mammals.... more We present unifying rules governing the efficient locomotion of swimming fish and marine mammals. Using scaling and dimensional analysis, supported by new experimental data, we show that efficient locomotion occurs when the values of the Strouhal (St) number St(=f A/U) and A * (=A/L), two nondimensional numbers that relate forward speed U , tail-beat amplitude A, tail-beat frequency f , and the length of the swimmer L are bound to the tight ranges of 0.2-0.4 and 0.1-0.3, respectively. The tight range of 0.2-0.4 for the St number has previously been associated with optimal thrust generation. We show that the St number alone is insufficient to achieve optimal aquatic locomotion, and an additional condition on A * is needed. More importantly, we show that when swimming at minimal power consumption, the Strouhal number of a cruising swimmer is predetermined solely by the shape and drag characteristics of the swimmer. We show that diverse species of fish and cetaceans cruise indeed with the St number and A * predicted by our theory. Our findings provide a physical explanation as to why fast aquatic swimmers cruise with a relatively constant tail-beat amplitude of approximately 20% of the body length, and their swimming speed is nearly proportional to their tail-beat frequency.
Genomic data can provide novel insights into the natural history of oceanic species. These data c... more Genomic data can provide novel insights into the natural history of oceanic species. These data can inform the management of vulnerable and slow-maturing species by estimating population structure, rates of migration, and the distribution of genetic diversity. In this study we focus on two protected elasmobranch species, the Winter Skate, Leucoraja ocellata, and the Little Skate, L. erinacea. We use genome-wide SNPs to estimate population structure, and quantify migration and genetic diversity among both species from four sampling localities across the Atlantic coast of North America. We find that species of Leucoraja are generally isolated by distance, although we infer some fine-scale population structure. Specifically, estimates of effective migration infer fine-scale population structure in L. ocellata between the northern sites of Georges Bank and the Mid-Atlantic sampling sites, whereas L. erinacea shows no evidence of population genetic structure in any analyses. We also found that genetic diversity is concentrated in the central sites of Georges Bank and the Mid-Atlantic Bight for L. ocellata, but is reduced at these two sites in L. erinacea, suggesting opposite distributions of genetic diversity between species. Thus, genomic data suggest that while species of Leucoraja lack discrete population structure, they likely employ only mid-range dispersal. These findings correspond to ecological studies that have found eco-physiological differences between embryonic and juvenile Leucoraja from different localities. Taken together, small-bodied skate research emphasizes the importance of local adaptive plasticity for marine species, even without population genetic structure. Conservation strategies should focus on managing the portions of the Atlantic coast considered most vital to reproduction of Leucoraja, but should not recognize multiple populations across their range.
Although linear accelerations are an important common component of the diversity of fish locomoto... more Although linear accelerations are an important common component of the diversity of fish locomotor behaviors , acceleration is one of the least-understood aspects of propulsion. Analysis of acceleration behavior in fishes with both spiny and soft-rayed median fins demonstrates that fin area is actively modulated when fish accelerate. We implemented an undulatory biomimetic robotic fish model with median fins manufactured using multimaterial three-dimensional printing-a spiny-rayed dorsal fin, soft-rayed dorsal/anal fins, and a caudal fin-whose stiffnesses span three orders of magnitude. We used an array of fluidic elastomeric soft actuators to mimic the dorsal/anal inclinator and erector/depressor muscles of fish, which allowed the soft fins to be erected or folded within 0.3 s. We experimentally show that the biomimetic soft dorsal/anal fin can withstand external loading. We found that erecting the soft dorsal/anal fins significantly enhanced the linear acceleration rate, up to 32.5% over the folded fin state. Surprisingly, even though the projected area of the body (in the lateral plane) increased 16.9% when the median fins were erected, the magnitude of the side force oscillation decreased by 24.8%, which may have led to significantly less side-to-side sway in the robotic swimmer. Visualization of fluid flow in the wake of median fins reveals that during linear acceleration, the soft dorsal fin generates a wake flow opposite in direction to that of the caudal fin, which creates propulsive jets with time-variant circulations and jet angles. Erectable/foldable fins provide a new design space for bioin-spired underwater robots with structures that morph to adapt to different locomotor behaviors. This biorobotic fish model is also a potentially promising system for studying the dynamics of complex multifin fish swimming behaviors, including linear acceleration, steady swimming, and burst and coast, which are difficult to analyze in freely swimming fishes.
Most batoids have a unique swimming mode in which thrust is generated by either oscillating or un... more Most batoids have a unique swimming mode in which thrust is generated by either oscillating or undulating expanded pectoral fins that form a disc. Only one previous study of the freshwater stingray has quantified three-dimensional motions of the wing, and no comparable data are available for marine batoid species that may differ considerably in their mode of locomotion. Here, we investigate three-dimensional kinematics of the pectoral wing of the little skate, Leucoraja erinacea, swimming steadily at two speeds [1 and 2 body lengths (BL) s −1 ]. We measured the motion of nine points in three dimensions during wing oscillation and determined that there are significant differences in movement amplitude among wing locations, as well as significant differences as speed increases in body angle, wing beat frequency and speed of the traveling wave on the wing. In addition, we analyzed differences in wing curvature with swimming speed. At 1 BL s −1 , the pectoral wing is convex in shape during the downstroke along the medio-lateral fin midline, but at 2 BL s −1 the pectoral fin at this location cups into the flow, indicating active curvature control and fin stiffening. Wing kinematics of the little skate differed considerably from previous work on the freshwater stingray, which does not show active cupping of the whole fin on the downstroke.
Indigenous red-bellied pacu, Piaractus brachypomus, populations are in decline due to overfishing... more Indigenous red-bellied pacu, Piaractus brachypomus, populations are in decline due to overfishing. Once ignored by aquaculturists because of their perceived low economic value, renewed aquaculture efforts in Central and South America aim to relieve fishing pressures on natural pacu populations. In the southern United States pacu aquaculture for the aquarium trade has raised concerns that accidental release could lead to establishment of overwintering populations outside captivity-a threat accentuated by the average 6 °C increase in shallow-water temperatures predicted by the end of the century. In the present study, Critical and Chronic Thermal Methodology was used to quantify red-bellied pacu thermal tolerance niche requirements. The data suggest that red-belllied pacu are a thermophilic species capable of tolerating low and high chronic temperatures of 16.5 °C and 35 °C, respectively. Critical thermal minimum and maximum temperatures of fish acclimated near their chronic limits are 10.3 and 44.4 °C. Red-bellied pacu aquaculture in the United States is concentrated in subtropical Florida regions that encourage rapid growth and reproduction, but carry an increased risk of establishing reproducing populations in local freshwater systems. The thermal niche data show that the risk of bioinvasion can be reduced or eliminated by adopting an approach whereby aquaculture potential is integrated with environmental temperature constraints.
Swimming performance is considered a key trait determining the ability of fish to survive. Hydrod... more Swimming performance is considered a key trait determining the ability of fish to survive. Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds and increasing expenditure at low and high speeds. However, to date no complete datasets have shown an energetic minimum for swimming fish at intermediate speeds rather than low speeds. To address this knowledge gap, we used a negatively buoyant fish, the clearnose skate Raja eglanteria, and took two approaches: a classic critical swimming speed protocol and a single-speed exercise and recovery procedure. We found an anaerobic component at each velocity tested. The two approaches showed U-shaped, though significantly different, speed-metabolic relationships. These results suggest that (i) postural costs, especially at low speeds, may result in J-or U-shaped metabolism-speed curves; (ii) anaerobic metabolism is involved at all swimming speeds in the clearnose skate; and (iii) critical swimming protocols might misrepresent the true costs of locomotion across speeds, at least in negatively buoyant fish. aerobic performance | critical swimming speed | elasmobranch | EPOC | swimming metabolic rate S wimming ability has no doubt contributed to the astonishing diversity and evolutionary success of fishes (1, 2), and efficiency of locomotion is a key measure of performance that influences reproduction, competition, foraging, and survival outcomes (3, 4). In fact, daily and seasonal movements allow fish to forage, reproduce, and find refuge from predators or abiotic stressors (5, 6). It comes as no surprise, therefore, that fish lo-comotion has been a productive research area for both evolutionary biologists and physiologists (4, 7-10). All fishes are capable of varying locomotor speed to some degree, and both the hydrodynamic mechanisms and energetic consequences of the species-specific use of propulsors (i.e., fins) have been investigated theoretically and experimentally (11-13). Vertebrate locomotor theory predicts that the total energetic requirements (or metabolic rate, _ MO 2) for steady swimming should vary with velocity, with the greatest expenditure at the lowest and highest sustainable speeds and minimum expenditure at intermediate speeds (4). This hypothesis is based on the assumption that during swimming, fish face perturbing forces and must stabilize their body posture to maintain direction (4, 14). As speed decreases, controlling stability becomes more difficult (15), and thus instability costs increase below optimal cruising speeds (14). For negatively buoyant fish, such a process involves a significant energy loss, because they also need to counteract gravity by accelerating water downward to create hydrodynamic lift (7, 16). At higher swimming speeds, energy expenditure increases significantly, as body drag is a function of velocity squared (17). Consequently, there is a range of intermediate velocities at which fish are expected to swim relatively economically , and these are typically identified as cruising speeds (4). Taken together, these different hydrodynamic forces acting on fishes during locomotion should result in the hypothetical nonlinear relationship (as either a J-shaped or a U-shaped curve) between speed and _ MO 2 (Fig. 1A). However, to date, we lack experimental measurements of energetic cost over a range of speeds sufficiently broad and in sufficient detail to support this theoretical model. This is especially surprising because the energetic cost of swimming has been assessed in many species of fish across a range of speeds. Instead, virtually all studies show that _ MO 2 increases with speed, with a minimum energetic cost at the lowest velocity tested (Fig. 1A). Testing swimming fish at very low speeds can be challenging, and thus fish energetic analyses have not generally provided data at low enough speeds to demonstrate increased energetic costs. One exception to this is recent work with a batoid fish, the little skate Leucoraja erinacea, which has demonstrated a unique relationship between speed and _ MO 2 (18). In that study, skates exhibited a decreasing _ MO 2 with increasing speed up to a relatively low optimal cruising velocity, but were unable to swim steadily beyond the optimal speed. In that case, locomotor performance was limited to the descending portion of a single metabolism speed relationship (18). Batoid fishes lack an expansive caudal fin and are unable to transition from paired fin to body and caudal fin locomotion, i.e., cannot switch gait, as is the case with many other aquatic vertebrates (16-18). Instead, they must rely on modified pectoral fins fused to the head, forming a disk to propel themselves at varying speeds (17, 19). Even though this extreme body plan is well adapted for a benthic life history, batoids are also able to swim up in the water column, and some species can even undertake large-scale migrations (20). Another notable conclusion of the previous study was the detection of a significant postexercise oxygen debt-a proxy for Significance Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds. Empirical studies to date do not support this view. Here we report a complete dataset on a swimming batoid fish that shows a clear energetic minimum at intermediate swimming speeds. We also demonstrate that this species uses a combination of aerobic and anaerobic metabolism to fuel steady swimming at each speed, including the slowest speeds tested. This contradicts the widespread assumption that fish use only aerobic metabolism at low speeds. Kinematic data support this nonlinear relationship by also showing a U-shaped pattern to body angle during steady swimming.
We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, th... more We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, the little skate, Leucoraja erinacea, at three swimming speeds. We report that this species has the lowest mass-adjusted swimming metabolic rate measured for any elasmobranch; however, this species incurs a much higher COT at approximately five times the lowest values recorded for some teleosts. In addition, because skates lack a propulsive caudal fin and could not sustain steady swimming beyond a relatively low optimum speed of 1.25 body lengths s −1 , we propose that the locomotor efficiency of benthic rajiform fishes is limited to the descending portion of a single COT-speed relationship. This renders these species poorly suited for long-distance translocation and, therefore, especially vulnerable to regional-scale environmental disturbances.
Ocean acidification and warming are known to alter, and in many cases decrease, calcification rat... more Ocean acidification and warming are known to alter, and in many cases decrease, calcification rates of shell and reef building marine invertebrates. However, to date, there are no datasets on the combined effect of ocean pH and temperature on skeletal mineralization of marine vertebrates, such as fishes. Here, the embryos of an oviparous marine fish, the little skate (Leucoraja erinacea), were developmentally acclimatized to current and increased temperature and CO 2 conditions as expected by the year 2100 (15 and 208C, approx. 400 and 1100 matm, respectively), in a fully crossed experimental design. Using micro-computed tomography, hydroxyapatite density was estimated in the mineralized portion of the cartilage in jaws, crura, vertebrae, denticles and pectoral fins of juvenile skates. Mineralization increased as a consequence of high CO 2 in the cartilage of crura and jaws, while temperature decreased mineralization in the pectoral fins. Mineraliz-ation affects stiffness and strength of skeletal elements linearly, with implications for feeding and locomotion performance and efficiency. This study is, to my knowledge, the first to quantify a significant change in min-eralization in the skeleton of a fish and shows that changes in temperature and pH of the oceans have complex effects on fish skeletal morphology.
We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, th... more We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, the little skate, Leucoraja erinacea, at three swimming speeds. We report that this species has the lowest mass-adjusted swimming metabolic rate measured for any elasmobranch; however, this species incurs a much higher COT at approximately five times the lowest values recorded for some teleosts. In addition, because skates lack a propulsive caudal fin and could not sustain steady swimming beyond a relatively low optimum speed of 1.25 body lengths s −1 , we propose that the locomotor efficiency of benthic rajiform fishes is limited to the descending portion of a single COT–speed relationship. This renders these species poorly suited for long-distance translocation and, therefore, especially vulnerable to regional-scale environmental disturbances.
Inspired by the relatively simple morphological blueprint provided by batoid fish such as stingra... more Inspired by the relatively simple morphological blueprint provided by batoid fish such as stingrays and skates, we created a biohybrid system that enables an artificial animal—a tissue-engineered ray—to swim and phototactically follow a light cue. By patterning dissociated rat cardiomyocytes on an elastomeric body enclosing a microfabricated gold skeleton, we replicated fish morphology at Embedded Image scale and captured basic fin deflection patterns of batoid fish. Optogenetics allows for phototactic guidance, steering, and turning maneuvers. Optical stimulation induced sequential muscle activation via serpentine-patterned muscle circuits, leading to coordinated undulatory swimming. The speed and direction of the ray was controlled by modulating light frequency and by independently eliciting right and left fins, allowing the biohybrid machine to maneuver through an obstacle course.
Elucidating the combined effects of increasing temperature and ocean acidification on performance... more Elucidating the combined effects of increasing temperature and ocean acidification on performance of fishes is central to our understanding of how species will respond to global climate change. Measuring the metabolic costs associated with intense and short activities, such as those required to escape predators, is key to quantifying changes in performance and estimating the potential effects of environmental stressors on survival. In this study, juvenile little skate Leucoraja erinacea from two neighboring locations (Gulf of Maine, or northern location, and Georges Bank, or southern location) were developmentally acclimatized and reared at current and projected temperatures (15, 18 or 20°C) and acidification conditions (pH 8.1 or 7.7), and their escape performance was tested by employing a chasing protocol. The results from this study suggest countergradient variation in growth between skates from the two locations, while the optimum for escape performance was at a lower temperature in individuals from the northern latitudes, which could be related to adaptation to the local thermal environment. Aerobic performance and scope declined in skates from the northern latitudes under simulated ocean warming and acidification conditions. Overall, the southern skates showed lower sensitivity to these climatic stressors. This study demonstrates that even mobile organisms from neighboring locations can exhibit substantial differences in energetic costs of exercise and that skates from the northern part of the geographic range may be more sensitive to the directional increase in temperature and acidification expected by the end of the century.
Climatic models have projected an increase in the frequency and intensity of heat waves and cold ... more Climatic models have projected an increase in the frequency and intensity of heat waves and cold events over the next century that have the potential to disrupt community dynamics, by reducing resilience of keystone species, such as cleaner fishes. One of the universal responses to global warming, together with shifts in geographic range and phenology, is the reduction of body size across taxonomic groups. As this phenomenon will likely play a major role in shaping communities, we investigate the effect of body size on acute thermal tolerance in cleaner gobies. In this study we set out to test the hypothesis that smaller fishes may be better able to tolerate acute temperature changes in the environment thus making them more resilient during extreme thermal events. We raised cleaner gobies of the genus Elacatinus (E. oceanops and the dwarf-sized E. lobeli) under common garden conditions and tested the effect of inter-individual variation in adult body size on thermal tolerance, using critical thermal methodology. Results from this study show that both species exhibit a limited capacity for acquired thermal tolerance following acclimation. Additionally, the smaller E. lobeli was able to tolerate higher and lower temperatures than E. oceanops. However, E. oceanops showed intraspecific difference in thermal tolerance, with smaller individuals being more thermo-tolerant. The comparison within these two species suggests that body size could have a role in thermo-tolerance and future physiological studies may test a range of sizes to capture the variation in responses of species and populations to temperature stress.
Fish Physiology and Biochemistry, 2011
In this study, flow-through respirometry was used to test the effect of acute temperature change ... more In this study, flow-through respirometry was used to test the effect of acute temperature change on resting routine metabolic rates of two benthic elasmobranchs, Atlantic stingrays, Dasyatis sabina (n = 7) and whitespotted bamboo sharks, Chiloscyllium plagiosum (n = 7) kept under fluctuating temperature regime of 24-27 and 23-25°C, respectively. Atlantic stingrays and whitespotted bamboo sharks showed a temperature sensitivity (Q 10 ) of 2.10 (21-31°C) and 2.08 (20-28°C), respectively. Not surprisingly, oxygen consumption (MO 2 ) increased in both species as temperature was raised. Acute increases in oxygen uptake may be useful during activities such as foraging, and some elasmobranchs may alter physiological processes by taking advantage of thermal variability in the environment. However, further investigation of different physiological processes is needed to better understand how temperature variation may affect behavioural choices of fishes.
International Conference on Artificial Intelligence, 2009
This paper presents the development of an application for digital image processing of x-rays of s... more This paper presents the development of an application for digital image processing of x-rays of stingrays. In order to measure the rate of absorption at varying temperatures, stingrays were fed detectable ball bearings. Using image processing techniques similar to digital mammography before the development of PACS, ball bearings and anchor points are detected in 111 scanned x-ray images of stingrays.
Journal of Fish Biology, 2011
The effects of post-feeding thermotaxis on ileum evacuation and absorption rates were examined in... more The effects of post-feeding thermotaxis on ileum evacuation and absorption rates were examined in the laboratory using two elasmobranch species, the Atlantic stingray Dasyatis sabina, which inhabits thermally variable environments, and the whitespotted bamboo shark Chiloscyllium plagiosum, a stenothermic fish living on Indo-Pacific reefs. Experiments at temperatures similar to those experienced in nature revealed temperature change had no significant effect on C. plagiosum absorption or evacuation rates, suggesting stenothermic sharks cannot exploit temperature differences as a means to improve digestion efficiency. On the other hand, D. sabina showed significantly lower evacuation and absorption rates at lower temperatures. The relative decrease was greater for evacuation (Q 10 = 3·08) than absorption rates (Q 10 = 2·20), resulting in a significant increase in total absorption, suggesting D. sabina can benefit from using shuttling behaviour to exploit thermal variability in their environment to maximize energetic uptake.
International Conference on Artificial Intelligence, 2009
This paper presents the development of an application for digital image processing of x-rays of s... more This paper presents the development of an application for digital image processing of x-rays of stingrays. In order to measure the rate of absorption at varying temperatures, stingrays were fed detectable ball bearings. Using image processing techniques similar to digital mammography before the development of PACS, ball bearings and anchor points are detected in 111 scanned x-ray images of stingrays.
We consider the propulsive performance of an unsteady heaving and bending foil with shape inspire... more We consider the propulsive performance of an unsteady heaving and bending foil with shape inspired by Thunniform swimmers such as tuna, computationally studying a parameter space of Strouhal Number and phase offsets between heave and bend motions. The phase offset í µí½ between the heaving and bending motions proves to be critical in determining the propulsive performance and flow structure of the fish-shaped panel. To maximize thrust, the heave and bend motions have to be almost in-phase but not completely (í µí½ ~ 330°), while to maximize efficiency, the bending motion needs to lag the heave motion by about one-fourth of period, which results in a motion of caudal fin at a modest angle of attack, which is similar to biology. I. Nomenclature í µí°´= µí°´= trailing edge amplitude í µí° ¶ í µí°¿ = lift coefficient í µí° ¶ í µí± = thrust coefficient í µí± = foil chord í µí± = foil span í µí±í µí±¡ = time step í µí± = frequency of motion ℎ = leading edge heave position í µí± ∞ = free stream velocity í µí±í µí±¡ = Strouhal number, í µí±í µí±¡ = 2í µí±í µí°´/í µí± ∞ í µí»¼ = angle of attack í µí¼ = propulsive effieciency, í µí¼ = í µí° ¶ í µí± /í µí° ¶ í µí± í µí¼ = pitch angle í µí¼ = kinematic viscosity í µí¼ = fluid density í µí¼ = phase angle between heave and bend motions
We present unifying rules governing the efficient locomotion of swimming fish and marine mammals.... more We present unifying rules governing the efficient locomotion of swimming fish and marine mammals. Using scaling and dimensional analysis, supported by new experimental data, we show that efficient locomotion occurs when the values of the Strouhal (St) number St(=f A/U) and A * (=A/L), two nondimensional numbers that relate forward speed U , tail-beat amplitude A, tail-beat frequency f , and the length of the swimmer L are bound to the tight ranges of 0.2-0.4 and 0.1-0.3, respectively. The tight range of 0.2-0.4 for the St number has previously been associated with optimal thrust generation. We show that the St number alone is insufficient to achieve optimal aquatic locomotion, and an additional condition on A * is needed. More importantly, we show that when swimming at minimal power consumption, the Strouhal number of a cruising swimmer is predetermined solely by the shape and drag characteristics of the swimmer. We show that diverse species of fish and cetaceans cruise indeed with the St number and A * predicted by our theory. Our findings provide a physical explanation as to why fast aquatic swimmers cruise with a relatively constant tail-beat amplitude of approximately 20% of the body length, and their swimming speed is nearly proportional to their tail-beat frequency.
Genomic data can provide novel insights into the natural history of oceanic species. These data c... more Genomic data can provide novel insights into the natural history of oceanic species. These data can inform the management of vulnerable and slow-maturing species by estimating population structure, rates of migration, and the distribution of genetic diversity. In this study we focus on two protected elasmobranch species, the Winter Skate, Leucoraja ocellata, and the Little Skate, L. erinacea. We use genome-wide SNPs to estimate population structure, and quantify migration and genetic diversity among both species from four sampling localities across the Atlantic coast of North America. We find that species of Leucoraja are generally isolated by distance, although we infer some fine-scale population structure. Specifically, estimates of effective migration infer fine-scale population structure in L. ocellata between the northern sites of Georges Bank and the Mid-Atlantic sampling sites, whereas L. erinacea shows no evidence of population genetic structure in any analyses. We also found that genetic diversity is concentrated in the central sites of Georges Bank and the Mid-Atlantic Bight for L. ocellata, but is reduced at these two sites in L. erinacea, suggesting opposite distributions of genetic diversity between species. Thus, genomic data suggest that while species of Leucoraja lack discrete population structure, they likely employ only mid-range dispersal. These findings correspond to ecological studies that have found eco-physiological differences between embryonic and juvenile Leucoraja from different localities. Taken together, small-bodied skate research emphasizes the importance of local adaptive plasticity for marine species, even without population genetic structure. Conservation strategies should focus on managing the portions of the Atlantic coast considered most vital to reproduction of Leucoraja, but should not recognize multiple populations across their range.
Although linear accelerations are an important common component of the diversity of fish locomoto... more Although linear accelerations are an important common component of the diversity of fish locomotor behaviors , acceleration is one of the least-understood aspects of propulsion. Analysis of acceleration behavior in fishes with both spiny and soft-rayed median fins demonstrates that fin area is actively modulated when fish accelerate. We implemented an undulatory biomimetic robotic fish model with median fins manufactured using multimaterial three-dimensional printing-a spiny-rayed dorsal fin, soft-rayed dorsal/anal fins, and a caudal fin-whose stiffnesses span three orders of magnitude. We used an array of fluidic elastomeric soft actuators to mimic the dorsal/anal inclinator and erector/depressor muscles of fish, which allowed the soft fins to be erected or folded within 0.3 s. We experimentally show that the biomimetic soft dorsal/anal fin can withstand external loading. We found that erecting the soft dorsal/anal fins significantly enhanced the linear acceleration rate, up to 32.5% over the folded fin state. Surprisingly, even though the projected area of the body (in the lateral plane) increased 16.9% when the median fins were erected, the magnitude of the side force oscillation decreased by 24.8%, which may have led to significantly less side-to-side sway in the robotic swimmer. Visualization of fluid flow in the wake of median fins reveals that during linear acceleration, the soft dorsal fin generates a wake flow opposite in direction to that of the caudal fin, which creates propulsive jets with time-variant circulations and jet angles. Erectable/foldable fins provide a new design space for bioin-spired underwater robots with structures that morph to adapt to different locomotor behaviors. This biorobotic fish model is also a potentially promising system for studying the dynamics of complex multifin fish swimming behaviors, including linear acceleration, steady swimming, and burst and coast, which are difficult to analyze in freely swimming fishes.
Most batoids have a unique swimming mode in which thrust is generated by either oscillating or un... more Most batoids have a unique swimming mode in which thrust is generated by either oscillating or undulating expanded pectoral fins that form a disc. Only one previous study of the freshwater stingray has quantified three-dimensional motions of the wing, and no comparable data are available for marine batoid species that may differ considerably in their mode of locomotion. Here, we investigate three-dimensional kinematics of the pectoral wing of the little skate, Leucoraja erinacea, swimming steadily at two speeds [1 and 2 body lengths (BL) s −1 ]. We measured the motion of nine points in three dimensions during wing oscillation and determined that there are significant differences in movement amplitude among wing locations, as well as significant differences as speed increases in body angle, wing beat frequency and speed of the traveling wave on the wing. In addition, we analyzed differences in wing curvature with swimming speed. At 1 BL s −1 , the pectoral wing is convex in shape during the downstroke along the medio-lateral fin midline, but at 2 BL s −1 the pectoral fin at this location cups into the flow, indicating active curvature control and fin stiffening. Wing kinematics of the little skate differed considerably from previous work on the freshwater stingray, which does not show active cupping of the whole fin on the downstroke.
Indigenous red-bellied pacu, Piaractus brachypomus, populations are in decline due to overfishing... more Indigenous red-bellied pacu, Piaractus brachypomus, populations are in decline due to overfishing. Once ignored by aquaculturists because of their perceived low economic value, renewed aquaculture efforts in Central and South America aim to relieve fishing pressures on natural pacu populations. In the southern United States pacu aquaculture for the aquarium trade has raised concerns that accidental release could lead to establishment of overwintering populations outside captivity-a threat accentuated by the average 6 °C increase in shallow-water temperatures predicted by the end of the century. In the present study, Critical and Chronic Thermal Methodology was used to quantify red-bellied pacu thermal tolerance niche requirements. The data suggest that red-belllied pacu are a thermophilic species capable of tolerating low and high chronic temperatures of 16.5 °C and 35 °C, respectively. Critical thermal minimum and maximum temperatures of fish acclimated near their chronic limits are 10.3 and 44.4 °C. Red-bellied pacu aquaculture in the United States is concentrated in subtropical Florida regions that encourage rapid growth and reproduction, but carry an increased risk of establishing reproducing populations in local freshwater systems. The thermal niche data show that the risk of bioinvasion can be reduced or eliminated by adopting an approach whereby aquaculture potential is integrated with environmental temperature constraints.
Swimming performance is considered a key trait determining the ability of fish to survive. Hydrod... more Swimming performance is considered a key trait determining the ability of fish to survive. Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds and increasing expenditure at low and high speeds. However, to date no complete datasets have shown an energetic minimum for swimming fish at intermediate speeds rather than low speeds. To address this knowledge gap, we used a negatively buoyant fish, the clearnose skate Raja eglanteria, and took two approaches: a classic critical swimming speed protocol and a single-speed exercise and recovery procedure. We found an anaerobic component at each velocity tested. The two approaches showed U-shaped, though significantly different, speed-metabolic relationships. These results suggest that (i) postural costs, especially at low speeds, may result in J-or U-shaped metabolism-speed curves; (ii) anaerobic metabolism is involved at all swimming speeds in the clearnose skate; and (iii) critical swimming protocols might misrepresent the true costs of locomotion across speeds, at least in negatively buoyant fish. aerobic performance | critical swimming speed | elasmobranch | EPOC | swimming metabolic rate S wimming ability has no doubt contributed to the astonishing diversity and evolutionary success of fishes (1, 2), and efficiency of locomotion is a key measure of performance that influences reproduction, competition, foraging, and survival outcomes (3, 4). In fact, daily and seasonal movements allow fish to forage, reproduce, and find refuge from predators or abiotic stressors (5, 6). It comes as no surprise, therefore, that fish lo-comotion has been a productive research area for both evolutionary biologists and physiologists (4, 7-10). All fishes are capable of varying locomotor speed to some degree, and both the hydrodynamic mechanisms and energetic consequences of the species-specific use of propulsors (i.e., fins) have been investigated theoretically and experimentally (11-13). Vertebrate locomotor theory predicts that the total energetic requirements (or metabolic rate, _ MO 2) for steady swimming should vary with velocity, with the greatest expenditure at the lowest and highest sustainable speeds and minimum expenditure at intermediate speeds (4). This hypothesis is based on the assumption that during swimming, fish face perturbing forces and must stabilize their body posture to maintain direction (4, 14). As speed decreases, controlling stability becomes more difficult (15), and thus instability costs increase below optimal cruising speeds (14). For negatively buoyant fish, such a process involves a significant energy loss, because they also need to counteract gravity by accelerating water downward to create hydrodynamic lift (7, 16). At higher swimming speeds, energy expenditure increases significantly, as body drag is a function of velocity squared (17). Consequently, there is a range of intermediate velocities at which fish are expected to swim relatively economically , and these are typically identified as cruising speeds (4). Taken together, these different hydrodynamic forces acting on fishes during locomotion should result in the hypothetical nonlinear relationship (as either a J-shaped or a U-shaped curve) between speed and _ MO 2 (Fig. 1A). However, to date, we lack experimental measurements of energetic cost over a range of speeds sufficiently broad and in sufficient detail to support this theoretical model. This is especially surprising because the energetic cost of swimming has been assessed in many species of fish across a range of speeds. Instead, virtually all studies show that _ MO 2 increases with speed, with a minimum energetic cost at the lowest velocity tested (Fig. 1A). Testing swimming fish at very low speeds can be challenging, and thus fish energetic analyses have not generally provided data at low enough speeds to demonstrate increased energetic costs. One exception to this is recent work with a batoid fish, the little skate Leucoraja erinacea, which has demonstrated a unique relationship between speed and _ MO 2 (18). In that study, skates exhibited a decreasing _ MO 2 with increasing speed up to a relatively low optimal cruising velocity, but were unable to swim steadily beyond the optimal speed. In that case, locomotor performance was limited to the descending portion of a single metabolism speed relationship (18). Batoid fishes lack an expansive caudal fin and are unable to transition from paired fin to body and caudal fin locomotion, i.e., cannot switch gait, as is the case with many other aquatic vertebrates (16-18). Instead, they must rely on modified pectoral fins fused to the head, forming a disk to propel themselves at varying speeds (17, 19). Even though this extreme body plan is well adapted for a benthic life history, batoids are also able to swim up in the water column, and some species can even undertake large-scale migrations (20). Another notable conclusion of the previous study was the detection of a significant postexercise oxygen debt-a proxy for Significance Hydrodynamic theory predicts that the energetic costs required for fishes to swim should vary with speed according to a U-shaped curve, with an expected energetic minimum at intermediate cruising speeds. Empirical studies to date do not support this view. Here we report a complete dataset on a swimming batoid fish that shows a clear energetic minimum at intermediate swimming speeds. We also demonstrate that this species uses a combination of aerobic and anaerobic metabolism to fuel steady swimming at each speed, including the slowest speeds tested. This contradicts the widespread assumption that fish use only aerobic metabolism at low speeds. Kinematic data support this nonlinear relationship by also showing a U-shaped pattern to body angle during steady swimming.
We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, th... more We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, the little skate, Leucoraja erinacea, at three swimming speeds. We report that this species has the lowest mass-adjusted swimming metabolic rate measured for any elasmobranch; however, this species incurs a much higher COT at approximately five times the lowest values recorded for some teleosts. In addition, because skates lack a propulsive caudal fin and could not sustain steady swimming beyond a relatively low optimum speed of 1.25 body lengths s −1 , we propose that the locomotor efficiency of benthic rajiform fishes is limited to the descending portion of a single COT-speed relationship. This renders these species poorly suited for long-distance translocation and, therefore, especially vulnerable to regional-scale environmental disturbances.
Ocean acidification and warming are known to alter, and in many cases decrease, calcification rat... more Ocean acidification and warming are known to alter, and in many cases decrease, calcification rates of shell and reef building marine invertebrates. However, to date, there are no datasets on the combined effect of ocean pH and temperature on skeletal mineralization of marine vertebrates, such as fishes. Here, the embryos of an oviparous marine fish, the little skate (Leucoraja erinacea), were developmentally acclimatized to current and increased temperature and CO 2 conditions as expected by the year 2100 (15 and 208C, approx. 400 and 1100 matm, respectively), in a fully crossed experimental design. Using micro-computed tomography, hydroxyapatite density was estimated in the mineralized portion of the cartilage in jaws, crura, vertebrae, denticles and pectoral fins of juvenile skates. Mineralization increased as a consequence of high CO 2 in the cartilage of crura and jaws, while temperature decreased mineralization in the pectoral fins. Mineraliz-ation affects stiffness and strength of skeletal elements linearly, with implications for feeding and locomotion performance and efficiency. This study is, to my knowledge, the first to quantify a significant change in min-eralization in the skeleton of a fish and shows that changes in temperature and pH of the oceans have complex effects on fish skeletal morphology.
We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, th... more We quantify the oxygen consumption rates and cost of transport (COT) of a benthic batoid fish, the little skate, Leucoraja erinacea, at three swimming speeds. We report that this species has the lowest mass-adjusted swimming metabolic rate measured for any elasmobranch; however, this species incurs a much higher COT at approximately five times the lowest values recorded for some teleosts. In addition, because skates lack a propulsive caudal fin and could not sustain steady swimming beyond a relatively low optimum speed of 1.25 body lengths s −1 , we propose that the locomotor efficiency of benthic rajiform fishes is limited to the descending portion of a single COT–speed relationship. This renders these species poorly suited for long-distance translocation and, therefore, especially vulnerable to regional-scale environmental disturbances.
Inspired by the relatively simple morphological blueprint provided by batoid fish such as stingra... more Inspired by the relatively simple morphological blueprint provided by batoid fish such as stingrays and skates, we created a biohybrid system that enables an artificial animal—a tissue-engineered ray—to swim and phototactically follow a light cue. By patterning dissociated rat cardiomyocytes on an elastomeric body enclosing a microfabricated gold skeleton, we replicated fish morphology at Embedded Image scale and captured basic fin deflection patterns of batoid fish. Optogenetics allows for phototactic guidance, steering, and turning maneuvers. Optical stimulation induced sequential muscle activation via serpentine-patterned muscle circuits, leading to coordinated undulatory swimming. The speed and direction of the ray was controlled by modulating light frequency and by independently eliciting right and left fins, allowing the biohybrid machine to maneuver through an obstacle course.
Elucidating the combined effects of increasing temperature and ocean acidification on performance... more Elucidating the combined effects of increasing temperature and ocean acidification on performance of fishes is central to our understanding of how species will respond to global climate change. Measuring the metabolic costs associated with intense and short activities, such as those required to escape predators, is key to quantifying changes in performance and estimating the potential effects of environmental stressors on survival. In this study, juvenile little skate Leucoraja erinacea from two neighboring locations (Gulf of Maine, or northern location, and Georges Bank, or southern location) were developmentally acclimatized and reared at current and projected temperatures (15, 18 or 20°C) and acidification conditions (pH 8.1 or 7.7), and their escape performance was tested by employing a chasing protocol. The results from this study suggest countergradient variation in growth between skates from the two locations, while the optimum for escape performance was at a lower temperature in individuals from the northern latitudes, which could be related to adaptation to the local thermal environment. Aerobic performance and scope declined in skates from the northern latitudes under simulated ocean warming and acidification conditions. Overall, the southern skates showed lower sensitivity to these climatic stressors. This study demonstrates that even mobile organisms from neighboring locations can exhibit substantial differences in energetic costs of exercise and that skates from the northern part of the geographic range may be more sensitive to the directional increase in temperature and acidification expected by the end of the century.
Climatic models have projected an increase in the frequency and intensity of heat waves and cold ... more Climatic models have projected an increase in the frequency and intensity of heat waves and cold events over the next century that have the potential to disrupt community dynamics, by reducing resilience of keystone species, such as cleaner fishes. One of the universal responses to global warming, together with shifts in geographic range and phenology, is the reduction of body size across taxonomic groups. As this phenomenon will likely play a major role in shaping communities, we investigate the effect of body size on acute thermal tolerance in cleaner gobies. In this study we set out to test the hypothesis that smaller fishes may be better able to tolerate acute temperature changes in the environment thus making them more resilient during extreme thermal events. We raised cleaner gobies of the genus Elacatinus (E. oceanops and the dwarf-sized E. lobeli) under common garden conditions and tested the effect of inter-individual variation in adult body size on thermal tolerance, using critical thermal methodology. Results from this study show that both species exhibit a limited capacity for acquired thermal tolerance following acclimation. Additionally, the smaller E. lobeli was able to tolerate higher and lower temperatures than E. oceanops. However, E. oceanops showed intraspecific difference in thermal tolerance, with smaller individuals being more thermo-tolerant. The comparison within these two species suggests that body size could have a role in thermo-tolerance and future physiological studies may test a range of sizes to capture the variation in responses of species and populations to temperature stress.
Fish Physiology and Biochemistry, 2011
In this study, flow-through respirometry was used to test the effect of acute temperature change ... more In this study, flow-through respirometry was used to test the effect of acute temperature change on resting routine metabolic rates of two benthic elasmobranchs, Atlantic stingrays, Dasyatis sabina (n = 7) and whitespotted bamboo sharks, Chiloscyllium plagiosum (n = 7) kept under fluctuating temperature regime of 24-27 and 23-25°C, respectively. Atlantic stingrays and whitespotted bamboo sharks showed a temperature sensitivity (Q 10 ) of 2.10 (21-31°C) and 2.08 (20-28°C), respectively. Not surprisingly, oxygen consumption (MO 2 ) increased in both species as temperature was raised. Acute increases in oxygen uptake may be useful during activities such as foraging, and some elasmobranchs may alter physiological processes by taking advantage of thermal variability in the environment. However, further investigation of different physiological processes is needed to better understand how temperature variation may affect behavioural choices of fishes.
International Conference on Artificial Intelligence, 2009
This paper presents the development of an application for digital image processing of x-rays of s... more This paper presents the development of an application for digital image processing of x-rays of stingrays. In order to measure the rate of absorption at varying temperatures, stingrays were fed detectable ball bearings. Using image processing techniques similar to digital mammography before the development of PACS, ball bearings and anchor points are detected in 111 scanned x-ray images of stingrays.
Journal of Fish Biology, 2011
The effects of post-feeding thermotaxis on ileum evacuation and absorption rates were examined in... more The effects of post-feeding thermotaxis on ileum evacuation and absorption rates were examined in the laboratory using two elasmobranch species, the Atlantic stingray Dasyatis sabina, which inhabits thermally variable environments, and the whitespotted bamboo shark Chiloscyllium plagiosum, a stenothermic fish living on Indo-Pacific reefs. Experiments at temperatures similar to those experienced in nature revealed temperature change had no significant effect on C. plagiosum absorption or evacuation rates, suggesting stenothermic sharks cannot exploit temperature differences as a means to improve digestion efficiency. On the other hand, D. sabina showed significantly lower evacuation and absorption rates at lower temperatures. The relative decrease was greater for evacuation (Q 10 = 3·08) than absorption rates (Q 10 = 2·20), resulting in a significant increase in total absorption, suggesting D. sabina can benefit from using shuttling behaviour to exploit thermal variability in their environment to maximize energetic uptake.
International Conference on Artificial Intelligence, 2009
This paper presents the development of an application for digital image processing of x-rays of s... more This paper presents the development of an application for digital image processing of x-rays of stingrays. In order to measure the rate of absorption at varying temperatures, stingrays were fed detectable ball bearings. Using image processing techniques similar to digital mammography before the development of PACS, ball bearings and anchor points are detected in 111 scanned x-ray images of stingrays.