Article

# Metabolism and Ram Gill Ventilation in Juvenile Paddlefish, Polyodon spathula (Chondrostei: Polyodontidae)

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## Abstract

Metabolic rate, branchial morphology, and modes of gill ventilation were studied in young (2-10 g) North American paddlefish, Polyodon spathula, with anatomical, behavioral, and physiological methods. Polyodon lacks the oral and opercular valves that are typical for fishes that rely on a buccal pump system to ventilate the gills, and the jaw opening system of Polyodon is poorly suited for regular pumping movements. Unrestrained, undisturbed juvenile paddlefishes swim constantly at a mean speed of 1.1-1.5 body lengths · $s^{-1}$ (bls). The maximum speed sustainable for > 10 min is 1.6-1.8 bls. When forced to swim at slow speeds in flow tanks or water tunnels, ventilation of the gills by buccal pumping occurs at a frequency of 50-80 · $min^{-1}$ . As swimming speed increases, buccal ventilation becomes intermittent and continuous ram ventilation occurs above 0.6-0.8 bls, which means that Polyodon is essentially an obligate ram ventilator under normal conditions. Oxygen consumption ( $\dot{M}O_{2}$ ), carbon dioxide production ( $\dot{M}O_{2}$ ), and the gas exchange ratio (R) were determined as a function of inspired Po₂ during undisturbed swimming in still water at 25° C Oxygen consumption, buccal pressure, and swimming performance were also measured at set swimming speeds in a flow tank and small water tunnel. Oxygen consumption at the preferred swimming speed of 1.25 bls was 6-7 μmol O₂, · $g^{-1}$ · $h^{-1}$ . Carbon dioxide production was 3-4 μmol CO₂ · $g^{-1}$ · $h^{-1}$ , yielding an R of 0.5-1.0. Paddlefishes are O₂ regulators in mild hypoxia (150 down to 90 mmHg) but die quickly at Po₂ < 90 mmHg. During steady swimming in normoxia, paddlefishes normally maintain 70%-80% of the maximum sustainable speed. This results in a normal minimum metabolic rate that is about twice that of the minimum (resting) rate of other acipensiform fishes. From a phylogenetic standpoint, other acipenseriforms also use ram ventilation, leading to the hypothesis that the evolutionary origin of a reliance on ram ventilation in Polyodon probably predates the origin of the filter feeding habit. Constant swimming may be metabolically expensive, but it would appear to allow some energy to be conserved by ram ventilation. This may be particularly advantageous for species such as P. spathula that combine filter feeding and ram ventilation.

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... Blockage, displacement, injury, or mortality of a fish can occur. Like other fish species, Paddlefish swimming abilities are influenced by behavior (Burggren and Bemis 1992), form, and size of fish (Hoover et al. 2009a(Hoover et al. , 2009b. As a result, flow fields can have variable effects on each individual fish. ...
... Swim studies provide considerable insight on intrinsic and extrinsic factors associated with Paddlefish locomotion. Swim speeds and metabolic rates of juveniles have been reported for ventilation and feeding and for variation in dissolved oxygen (Burggren and Bemis 1992;Sanderson et al. 1994;Aboagye and Allen 2014). Paddlefish metabolism, although less temperature-dependent than that other fishes, is significantly different and appreciable over a temperature range of 10-30°C (Patterson et al. 2013;Cage 2015) and has been implicated in the compressed life cycles of southern populations (Scarnecchia et al. 2011). ...
... Temperature effects on locomotion, however, are uncertain. Lethargic swimming has been observed at temperatures <5°C (Scarnecchia et al. 2011) but swim speeds of juveniles at 18 and 26°C were not significantly different (Aboagye and Allen 2014), and most performance studies are conducted within the narrower range of 20-25°C (Tomljanovich et al. 1977;Burggren and Bemis 1992;Hoover et al. 2009b). Consequently, it is not possible at this time to describe a temperature-swimming relationship. ...
Chapter
Paddlefish, Polyodon spathula, are behaviorally, morphologically, and physiologically adapted for prolonged free-swimming at moderately high speeds but not for maneuverability which makes them prone to impacts from submerged structures. These structures include low-head dams, weirs, dikes, levees, high-head dams, dredges, diversions, intakes, and vessels. Impacts include blocked migrations, reduced access and quality of habitat, entrainment, impingement, trauma, and stranding. Effects of these impacts on individuals are displacement, injuries, and death; effects on populations are fragmentation, lower gene flow, lower reproductive success, and elevated rate of mortality. Despite this, the status of the Paddlefish in most parts of its historic range is secure. Management techniques, like stocking and habitat restoration, are typically implemented at the local level but appear effective at conserving the species range wide. Refinement of management techniques, however, is still possible by modifying operations of structures and by rescuing stranded Paddlefish
... The model's three anterior arches extended from the ventral midline to the dorsal midline, and the fourth branchial arches extended only over the ventral portion of the model (Burggren and Bemis, 1992). To simulate gill rakers, the model's gill slots were covered with a nylon mesh ( pore diameter 140 µm, thread diameter 50 µm, 55% open pore area; Component Supply Co., Fort Meade, FL, USA). ...
... Sanderson et al. (1994), in the only known flow speed recordings taken from the interior of the oral cavity of live, ram suspension-feeding fish, showed that the flow speed measured during paddlefish suspension feeding (22-29 cm EFL) fluctuated at regular time intervals, though the cause of these fluctuations was not investigated at the time. Also, Burggren and Bemis (1992) recorded buccal pressure in a paddlefish (13.0 cm fork length) during ram ventilation and ventilation by buccal pumping, noting that pressure oscillations during ram ventilation reflected tailbeats. ...
... Future experiments could quantify the effects of different prey and prey concentrations on time to clogging in 3D models and on feeding bout duration in live ram suspension-feeding fish. Burggren and Bemis (1992) reported that paddlefish ram suspension feeding occurred 'in bursts of variable duration', and feeding bouts ranging from approximately 5 to 45 s have been observed (S.L.S., personal observation). In the videos that we used to quantify the swimming kinematics of paddlefish, the longest recorded uninterrupted bout of ram suspension feeding on adult brine shrimp, rather than brine shrimp cysts as we used in our flow tank experiments, was approximately 10 s. ...
Article
Ram suspension-feeding fishes swim with an open mouth to force water through the oral cavity and extract prey items that are too small to be pursued individually. Recent research has indicated that, rather than using a dead-end mechanical sieve, American paddlefish (Polyodon spathula Walbaum) employ vortical cross-step filtration. In this filtration mechanism, vortical flow that is generated posterior to the branchial arches organizes crossflow filtration processes into a spatial structure across the gill rakers. Despite the known impact of locomotor kinematics on fluid flow around the bodies of swimming fish, the effects of locomotor kinematics on filtration mechanisms in ram suspension feeders are unknown. Potential temporal organization of filtration mechanisms in ram suspension-feeding fish has not been studied previously. We investigated the effects of locomotor kinematics associated with undulatory swimming on intra-oral flow patterns and food particle transport. A mechanized model of the oral cavity was used to simulate the swimming kinematics of suspension-feeding paddlefish. We recorded fluctuations of flow speed and pressure within the model, which occurred at a frequency that corresponded with the frequency of the model's strides. Using the mechanized model in a flow tank seeded with Artemia cysts, we also showed that swimming kinematics aided the transport of this simulated food to the posterior margins of the gill slots, although the time scale of this transport is expected to vary with prey parameters such as size and concentration. Dye stream experiments revealed that, while stable vortical flow formed due to flow separation downstream of backward-facing steps in control trials, vortical flow structures in mechanized trials repeatedly formed and shed. These findings suggest strong integration between locomotor and feeding systems in ram suspension-feeding fishes.
... Eutrophication has been associated with hypoxia-related fish kills and corresponding loss of sensitive species in many aquatic systems around the world (Diaz and Breitburg 2009). Available information indicates that American paddlefish are obligatory ram ventilators and oxyregulators with a relatively high metabolic rate and sensitivity to hypoxia, with a minimum oxygen requirement of >2 mg/L (Burggren and Bemis 1992;Patterson et al. 2013;Aboagye and Allen 2014). Because paddlefish are obligatory ram ventilators, they do not undergo metabolic depression to the degree observed in sturgeons when exposed to hypoxia (Burggren and Bemis 1992;Crocker and Cech 1997;Aboagye and Allen 2014). ...
... Available information indicates that American paddlefish are obligatory ram ventilators and oxyregulators with a relatively high metabolic rate and sensitivity to hypoxia, with a minimum oxygen requirement of >2 mg/L (Burggren and Bemis 1992;Patterson et al. 2013;Aboagye and Allen 2014). Because paddlefish are obligatory ram ventilators, they do not undergo metabolic depression to the degree observed in sturgeons when exposed to hypoxia (Burggren and Bemis 1992;Crocker and Cech 1997;Aboagye and Allen 2014). Similar to other acipenseriforms, paddlefish lack the RBC pH protecting beta adrenergic Na + /H + exchanger (βNHE; Berenbrink et al. 2005;Regan and Brauner 2010). ...
... Therefore, the decrease in blood pO 2 and the elevation in blood pCO 2 , and glucose and lactate concentrations after acute moderate and extreme hypoxia exposure suggest that hyperventilation was not an effective response, causing a switch to anaerobic metabolism to compensate for the loss of aerobic energy production (Holeton and Randall 1967). Paddlefish have been observed to have a pO 2crit (pO 2 at which fish switch to anaerobic metabolism, because aerobic metabolic demand cannot be sustained by ambient pO 2 ) of 74-90 mmHg (Burggren and Bemis 1992;Aboagye and Allen 2014). This pO 2crit is higher than those reported for other relatively hypoxia-sensitive species such as Adriatic sturgeon, Acipenser naccarri (McKenzie et al. 2007), Siberian sturgeon, A. baeri (Nonnotte et al. 1993), and rainbow trout (Ott et al. 1980). ...
Article
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Despite the increasing prevalence of hypoxia in natural habitats occupied by the American paddlefish, basal bony fish, and ram ventilator, information about its response to hypoxia is scarce. To understand the physiological and biochemical responses of juvenile paddlefish (~150 g) to acute (<24 h) and chronic hypoxia (≥24 h), blood oxygen transport, blood acid-base balance, and metabolic stress were evaluated under four different partial pressures of oxygen [pO2; normoxia (148 mmHg), mild hypoxia (89 mmHg), moderate hypoxia (59 mmHg), and extreme hypoxia (36 mmHg)], all at 21 °C. Arterial blood samples were collected from paddlefish after they had been exposed to treatments for 0.25, 2, 6, 24, and 72 h, and analyzed for hematocrit, pO2, total oxygen content, oxygen saturation, pCO2, pH, hemoglobin, Na(+), K(+), Ca(2+), Cl(-), glucose, and lactate. Mild hypoxia only caused a reduction in blood pO2 and oxygen saturation. Both acute and chronic moderate and extreme hypoxia caused a decrease in blood pH, pO2, total oxygen content, plasma Na(+), and Cl(-) at all time points. Acute moderate and extreme hypoxia resulted in an increase in blood pCO2, plasma glucose, lactate, and hematocrit. Chronic exposure to moderate hypoxia resulted in an increase in plasma lactate, red blood cell count, and hemoglobin. This study shows that paddlefish are able to physiologically compensate for mild hypoxia, but exhibit secondary stress responses and are unable to return to homeostasis when exposed to both acute and chronic moderate hypoxia, and die after 3-8 h of extreme hypoxia.
... spathula. The studies that exist worked primarily with juveniles (Burggren & Bemis, 1992;Sanderson et al., 1994). This study used a wide range of P . ...
... No reduction in respiration rate was observed before the 3·75 mg · l −1 low oxygen threshold as P . spathula are oxyregulators until near the fatal degree of hypoxia (Burggren & Bemis, 1992). The temperature increase from 10 to 20 • C significantly increased routine oxygen consumption in small (Q 10 = 1·76), medium (Q 10 = 1·54) and large (Q 10 = 1·71) fish. ...
... A publication which measured respiration in P . spathula (Burggren & Bemis, 1992), however, was not included in Table III because fish masses (2-10 g) were at least a factor of 5 lower than the smallest fish used in the model from this study. Fish in this study were functioning in a state of routine aerobic metabolism because external stimuli were reduced to the greatest extent possible and animals swam with only enough velocity to respire. ...
Article
This study quantified the effects of temperature and fish mass on routine metabolism of the American paddlefish Polyodon spathula. Thermal sensitivity, as measured by Q10 value, was low in P. spathula. Mean Q10 was 1·78 while poikilotherms are generally expected to have Q10 values in the 2·00-2·50 range. Mass-specific metabolism did not decrease with increased fish size to the extent that this phenomenon is observed in teleosts, as evidenced by a mass exponent (β) value of 0·92 for P. spathula compared with 0·79 in a review of teleost species. Other Acipenseriformes have exhibited relatively high β values for mass-specific respiration. Overall P. spathula metabolism appears to be more dependent on body mass and less dependent on temperature than for many other fishes. An equation utilizing temperature and fish mass to estimate gross respiration for P. spathula was derived and this equation was applied to respiratory data from other Acipenseriformes to assess inter-species variation. Polyodon spathula respiration rates across water temperature and fish mass appear most similar to those of Atlantic sturgeon Acipenser naccarii and white sturgeon Acipenser transmontanus.
... At water temperatures of 22 • C, the paddlefish is reported to be in continuous motion and an obligate ram ventilator, with a metabolic rate of about twice that of the resting metabolic rate of other Acipenseriformes, none of which are obligate ram ventilators, although some may be capable of ram ventilation (Burggren and Bemis, 1992). It has been observed that paddlefish of all sizes (3-4 cm in length through 40-kg adults) at 20 • C are in continuous motion, as they ram ventilate and seek food through particulate feeding (primarily age 0 fish; Fredericks, 1994) or, most commonly, filter-feeding (Rosen and Hales, 1981;Michaletz et al., 1982;Burggren and Bemis, 1992). ...
... At water temperatures of 22 • C, the paddlefish is reported to be in continuous motion and an obligate ram ventilator, with a metabolic rate of about twice that of the resting metabolic rate of other Acipenseriformes, none of which are obligate ram ventilators, although some may be capable of ram ventilation (Burggren and Bemis, 1992). It has been observed that paddlefish of all sizes (3-4 cm in length through 40-kg adults) at 20 • C are in continuous motion, as they ram ventilate and seek food through particulate feeding (primarily age 0 fish; Fredericks, 1994) or, most commonly, filter-feeding (Rosen and Hales, 1981;Michaletz et al., 1982;Burggren and Bemis, 1992). Fish stationary in rivers position themselves in places where water can flow actively across their gills. ...
... During the summer growing season, rearing in reservoirs and backwaters, where zooplantivorous food is more abundant, predominates over river and main channel residency. It was observed that when paddlefish are confined in 20 • C water in tanks too small for the fish to actively swim or turn (thus preventing continuous forward movement and ram ventilation), the fish will list after less than a minute, consistent with results of Burggren and Bemis (1992) of obligatory ram ventilation at 22 • C. No specific information has been found on the necessity of ram ventilation at water temperatures near freezing. ...
Article
Full-text available
Sampling conducted in 2008–2010 on a southern Great Plains stock of paddlefish Polyodon spathula inhabiting the Neosho River, Spring River, and Grand Lake, Oklahoma, is characterized (1) in terms of the Acipenseriform life history framework outlined for the Yellowstone–Sakakawea stock of the Northern Plains and (2) in relation to the framework metabolic theory of ecology and associated latitudinal and environmental correlations with lifespan. In the Grand Lake stock, male fish typically mature at ages 6–7, and females mature at ages 8–9. The five stages of the lifespan (immature, maturing, growth and reproduction, prime reproduction, senescence to death) are compressed into a period of 15–20 years; the prime reproduction period occurs from ages 12 to 16 years for females. This lifespan compares to one of 40–50 years (and occasionally longer), and a prime reproduction period for females from ages 25 to 40 years, for the Yellowstone–Sakakawea stock. The more compressed lifespan of the Grand Lake stock and lower energy storage, as indicated by weights of gonadal fat bodies, are consistent with the framework metabolic theory of ecology. Over the course of a year, fish in Grand Lake are under a much higher metabolic demand than those in Lake Sakakawea. The distinct differences detailed between these two stocks from the southern and northern plains may exist between other paddlefish stocks, other Acipenseriform species, and other fish taxa separated by large latitudinal and climatic differences. The results have specific implications for harvest management and effects of climate change on Acipenseriform life histories and lifespan.
... The filter-feeding strategy in P. spathula requires extensive foraging activity. Burggren and Bemis (1992) demonstrated that the constant spontaneous swimming observed in Polyodon reflects an adaptation for ram ventilation of the gills that, presumably, coevolved with the filter-feeding lifestyle. In juvenile paddlefish at 25 C, the transition to complete ram ventilation occurred at about 50% of U crit (Table 7.3) and the speed of spontaneous swimming activity was 70-80% of U crit (Burggren and Bemis, 1992). ...
... Burggren and Bemis (1992) demonstrated that the constant spontaneous swimming observed in Polyodon reflects an adaptation for ram ventilation of the gills that, presumably, coevolved with the filter-feeding lifestyle. In juvenile paddlefish at 25 C, the transition to complete ram ventilation occurred at about 50% of U crit (Table 7.3) and the speed of spontaneous swimming activity was 70-80% of U crit (Burggren and Bemis, 1992). Aerobic scope was similar to sturgeon (Table 7.4) but metabolic rate rose very rapidly as swimming speed increased and, given that the juvenile paddlefish swam spontaneously at speeds close to their U crit , they appeared to operate routinely in the upper portion of their aerobic scope for activity (Burggren and Bemis, 1992;Peake, 2004). ...
... In juvenile paddlefish at 25 C, the transition to complete ram ventilation occurred at about 50% of U crit (Table 7.3) and the speed of spontaneous swimming activity was 70-80% of U crit (Burggren and Bemis, 1992). Aerobic scope was similar to sturgeon (Table 7.4) but metabolic rate rose very rapidly as swimming speed increased and, given that the juvenile paddlefish swam spontaneously at speeds close to their U crit , they appeared to operate routinely in the upper portion of their aerobic scope for activity (Burggren and Bemis, 1992;Peake, 2004). Burggren and Bemis (1992) suggested that, although this might indicate an energetically expensive lifestyle, it would allow some energy to be conserved by ram ventilation. ...
Article
Swimming is critical to the ecology of many fishes as it determines, for example, their ability to forage, to escape predators, and to migrate. The information about locomotion in primitive fishes is, however, sparse and unevenly distributed. For example, sustained exercise performance has been studied in the primitive groups with a migratory lifestyle such as lampreys and sturgeons, whereas fast‐start performance has been investigated in sit‐and‐wait predators such as the bichirs and gars. Very little is known about locomotion in lungfishes, typically considered rather sedentary species. The lamprey has been a model for studies of the neural circuits that drive axial locomotion, but this information has yet to be put into a clear evolutionary context relative to other fishes. Indeed, there have been relatively few studies aimed explicitly at investigating the evolution of locomotor performance in primitive fishes, aside from some studies on startle behaviors. Great caution should be exercised when making literature‐based comparisons between “the teleosts” and single primitive species, or discrete phylogenetic groups with particular life histories and morphologies (e.g., sturgeons). The evidence does indicate, however, that primitive fishes perform exercise less well than teleosts with similar lifestyles. This is true for swimming endurance, critical speed swimming, and fast starts. Thus, the evolution of fishes to the teleosts has, in fact, been associated with evolution of “better” exercise performance. It is tempting to speculate that improved locomotor ability might have contributed to the dominance of the teleosts today.
... Small differences in buccal pressure occur as the tails of paddlefishes oscillate, though the exact importance of these differences is unclear as of yet (Burggren and Bemis 1992). At slow swimming speeds, buccal pumping is employed to get adequate oxygen into the blood, but the complete absence of swimming puts these fishes in distress. ...
... This indicates that the slight pressure differences caused by tail movements may be necessary for adequate gas exchange in these species. At faster speeds, paddlefish wholly use ram ventilation, meaning caudal fin movements are entirely relied upon in order to respire (Burggren and Bemis 1992;Haines and Sanderson 2017). In terms of overall steady swimming, the kinematics of locomotion in paddlefish is not well studied. ...
Article
Fishes are the longest persisting living vertebrates and as such, display an incredible array of diversity. Variation in the tail, or caudal fin, is often a reflection of a fish's environment, and affects movement, predation, defense, and reproduction. Previous literature has discussed many aspects of caudal fin form and function in particular taxonomic groups; however, no previous work has synthesized these studies in order to detail how the caudal fin is structured, and what purpose this structure serves, throughout the phylogeny of fishes. This review examines the caudal fin throughout the main lineages of fish evolution, and highlights where changes in shape and usage have occurred. Such novelties in form and function tend to have far-reaching evolutionary consequences. Through integration of past and present work, this review creates a coherent picture of caudal fin evolution. Patterns and outliers that demonstrate how form and function of this appendage are intertwined can further inform hypotheses that fill critical gaps in knowledge concerning the caudal fin.
... Filter-feeding in paddlefish varies in duration and speed of swimming. The mouth is stretched fully open for maximum filtration surface and the branchial (gill) arches and opercular flaps are spread, while the paddlefish swims forward to catch planktonic prey (Burggren and Bemis 1992;Rosen and Hales 1981). As a result of this forward swimming motion, the water enters continuously (and not in separate 'bites'), thus known as ram filter-feeding. ...
... During buccal pumping water needs to be pumped over the gill filaments, whereas during ram ventilation the forward motion of the fish ensures water flow over the gill filaments. Forward swimming in combination with open gills increases drag due to the resistance of the gills in the water (Burggren and Bemis 1992). This suggests that ram ventilation is energetically costly when foraging. ...
Article
The American paddlefish (Polyodon spathula) uses ram filter-feeding to forage for (mainly) zooplankton throughout the water column. It makes an ontogenetic transition from buccal pumping to ram ventilation feeding in the first year. In wild conditions, plankton is often distributed unevenly in time and space; however, this does not always apply to captive conditions. In the present study, two paddlefish were fed on a range of diets and supply methods to investigate the effect on foraging strategy. Insight into influencing foraging strategies could be beneficial for zoos and aquaria for display purposes or for improving welfare conditions. The paddlefish were studied during foraging, and foraging strategy, bout length and usage of the aquarium space were recorded. Three foraging strategies can be distinguished: foraging while swimming in straight lines, foraging while swimming in circulatory paths and particulate foraging. Although these strategies appear to not have a fixed switch-point, a significant difference was found between the foraging strategies for start and end points of certain strategies in relation to food density (P<0.003). Mean time spent on a strategy differed in duration from 1 to 60 seconds. When negative buoyant food sources (e.g. Mysids) were used, the paddlefish foraged in the lower parts of the aquarium. Neutrally buoyant food sources (e.g. Daphnia pulex) caused the paddlefish to forage throughout different depths of the aquarium (P<0.001).
... Subsequent alteration of rivers via channelization and impoundment (reservoirs, lock-and-dam structures), especially in the upper Mississippi River, is also likely a principal factor associated with rangewide declines (Carlson and Bonislawsky 1981). In addition, public perception of Paddlefish as a rough fish and as a competitor with game fish prompted some state agencies to control populations in the southern United States (e.g., Bryan 1942;Cottrell 1944). By the 1970s, populations had disappeared from the Great Lakes and eastern states, and Paddlefish were abundant only in parts of the Mississippi River drainage. ...
... Its more than 40,000 ampullae of Lorenzini (Allis 1903;Kistler 1906;Jørgensen et al. 1972) make it an antennae for nonvisual (vibration and electrical) signals given off by the zooplankton on which the Paddlefish feeds (New and Bodznick 1985;Wilkens et al. 1997). Paddlefish swim continuously at moderate to fast speeds (1-4 body lengths/s) and are capable of moving great distances in short times (Burggren and Bemis 1992;Hoover et al. 2009b;Hoover et al. 2013;Patterson et al. 2013). These movements, along with their rapid growth and large size (Adams 1942; Reed et al. 1992), are energetically costly. ...
... A lthough more than 70 species of suspension-feeding fishes compose 25% of the world fish catch, the fluid dynamic processes enabling fish to avoid clogging of the gill-raker filter are unknown. Not only does their gill-raker filter remain free from particle accumulation, suspension-feeding fishes are also able to retain and concentrate particles that are smaller than the filter pores and can even retain particles when large regions of the gill-raker filter are absent [1][2][3][4][5] . In addition to the ecological and evolutionary relevance, these problems are of substantial interest to industrial filtration engineers who seek to reduce the major operating expenses associated with clogging 6 . ...
... Industrial crossflow filtration is performed at transmembrane pressures that are 1-4 orders of magnitude higher 48 . The surprising performance of the cross-step filter despite an incomplete mesh is consistent with previously unexplained reports of basking shark and young paddlefish suspension feeding with only partially developed gill rakers 4,5 . ...
Article
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Suspension-feeding fishes such as goldfish and whale sharks retain prey without clogging their oral filters, whereas clogging is a major expense in industrial crossflow filtration of beer, dairy foods and biotechnology products. Fishes' abilities to retain particles that are smaller than the pore size of the gill-raker filter, including extraction of particles despite large holes in the filter, also remain unexplained. Here we show that unexplored combinations of engineering structures (backward-facing steps forming d-type ribs on the porous surface of a cone) cause fluid dynamic phenomena distinct from current biological and industrial filter operations. This vortical cross-step filtration model prevents clogging and explains the transport of tiny concentrated particles to the oesophagus using a hydrodynamic tongue. Mass transfer caused by vortices along d-type ribs in crossflow is applicable to filter-feeding duck beak lamellae and whale baleen plates, as well as the fluid mechanics of ventilation at fish gill filaments.
... Estimated relative swim-speeds, in body lengths per second, bls-1 (i.e., absolute swim-speed in cm/s divided by the EFL in cm), were 1.0-2.1 bls-1. These values are comparable to or lower than sustained swim-speeds of juvenile Paddlefish <90 mm EFL, which range from 1.1 to >4 bls-1 (Burggren andBemis 1992, Hoover et al. 2009a). ...
... Passage periods, in calendar dates, assume uniform net upriver movement of 2.5 km/day (2.9 cm/s) and are proportionate to length of reach. River velocities (cm/s) are based on average or mean (SD) velocity for corresponding dates (USACE, 2012b (Burggren and Bemis 1992) and from exposure to temperatures >28 °C, which are considered unsuitable for adult Paddlefish (Crance 1987). This Paddlefish was able to recover following capture, likely due in part to our judicious handling and its prompt release. ...
Article
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We observed a large adult Paddlefish entrained from the Mississippi River through the Bonnet Cane spillway, south Louisiana, which was injured and underweight. We captured, measured (23 metrics), and tagged the fish. After it had spent a week at large on the fioodway, we recaptured and released it back into the Mississippi River. The specimen was re-captured eight months later in northern Mississippi, 627 km upriver from where it was released. Distance traveled and water velocities in the river indicate that the fish was traveling at least 90-197 cm/s for prolonged periods, equivalent to gross speeds of 77-170 km/d. This incident suggests that a large entrained fish, trapped for several days in a hyperthermic and hypoxic habitat, can be viable when returned to the river. It also demonstrated that rescue efforts could reduce impacts of spillway operations to fish populations, and that comprehensive field assessment of fish morphology can be benign to fish.
... Sturgeons and paddlefishes are strictly water‐breathers , unlike many of the other primitive fishes , and the gills possess filaments with relatively well‐ developed lamellae that are similar to those of teleost fishes . Paddlefishes are filter feeders , and juvenile Polyodon spathula are obligate ram‐ventilators in normoxia and swim continuously shortly following hatch and throughout life ( Burggren and Bemis , 1992 ) . While they have the ability to ventilate their gills at low swimming speeds ( <0 . ...
... 6 – 0 . 8 body lengths s À1 ) , juveniles are not tolerant of hypoxia and die at a PwO 2 < 90 mmHg ( Burggren and Bemis , 1992 ) . The paddlefishes have reduced scales , and thus transcutaneous gas transfer may occur ; however , this has not been measured directly . ...
Article
Gas exchange is a prerequisite of vertebrate life. In terms of structural and functional diversity and habitats occupied, extant teleosts clearly outcompete extant primitive fishes; however, there are a few aspects related to gas exchange that may have contributed to the survival of these primitive fishes. Most of the primitive fishes either have the ability to breath air, have the ability to tolerate aerial exposure (and in some cases estivate), or are tolerant to aquatic hypoxia. Many of the bimodal breathers retain fully functional gills, which at times allow strictly aquatic breathing over prolonged periods which may be important for aerial predator avoidance or surviving ice cover in temperate climates. While air breathing is important for surviving aquatic hypoxia, it is also important in enhancing O2 uptake during exercise. Living primitive fishes occupy strategic positions in the evolutionary tree of vertebrates and may shed light on the evolution of blood O2 and CO2 transport characteristics. Evolutionary reconstruction indicates that the increase in the Bohr–Haldane effect in primitive ray‐finned fishes was followed first by a gradual increase in the magnitude of the Root effect and then a gradual reduction in specific Hb buffer value. This was followed by the evolution of a choroid rete mirabile and ocular O2 secretion in the last common ancestor of Amia calva and teleosts. Finally, the adrenergic red blood cell Na+/H+ exchanger was never present in primitive ray‐finned fishes or primitive teleosts and only evolved in advanced teleosts. No such evolutionary trends are observed in primitive lobe‐finned fishes.
... A similar conclusion was reached by Heath (475) for ventilation amplitude (measured as buccal or opercular pressure) versus frequency in rainbow trout. At higher swimming velocities, a transition from active breathing to ram ventilation occurs in many but not all fish species (141,206,364,475,982,1086). This strategy transfers the work of breathing from the ventilatory to the locomotory muscles, with an accompanying reduction in the energetic cost of O 2 delivery to the gill (364,365,1086). ...
Chapter
The ectothermic vertebrates are a diverse group that includes the Fishes (Agnatha, Chondrichthyes, and Osteichthyes), and the stem Tetrapods (Amphibians and Reptiles). From an evolutionary perspective, it is within this group that we see the origin of air-breathing and the transition from the use of water to air as a respiratory medium. This is accompanied by a switch from gills to lungs as the major respiratory organ and from oxygen to carbon dioxide as the primary respiratory stimulant. This transition first required the evolution of bimodal breathing (gas exchange with both water and air), the differential regulation of O2 and CO2 at multiple sites, periodic or intermittent ventilation, and unsteady states with wide oscillations in arterial blood gases. It also required changes in respiratory pump muscles (from buccopharyngeal muscles innervated by cranial nerves to axial muscles innervated by spinal nerves). The question of the extent to which common mechanisms of respiratory control accompany this progression is an intriguing one. While the ventilatory control systems seen in all extant vertebrates have been derived from common ancestors, the trends seen in respiratory control in the living members of each vertebrate class reflect both shared-derived features (ancestral traits) as well as unique specializations. In this overview article, we provide a comprehensive survey of the diversity that is seen in the afferent inputs (chemo and mechanoreceptor), the central respiratory rhythm generators, and the efferent outputs (drive to the respiratory pumps and valves) in this group. © 2022 American Physiological Society. Compr Physiol 12: 1-120, 2022.
... This has important implications for the interpretation of the morphologically similar spiracular region in tetrapodomorph fishes (see below). By contrast, the small spiracles of sturgeons and paddlefishes seem to have no respiratory function (Burggren, 1978;Burggren and Bemis, 1991). In neopterygians (gars, bowfins and teleosts) the spiracles are vestigial or absent, although the pseudobranch often persists inside the gill chamber. ...
Article
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The spiracular region, comprising the hyomandibular pouch together with the mandibular and hyoid arches, has a complex evolutionary history. In living vertebrates, the embryonic hyomandibular pouch may disappear in the adult, develop into a small opening between the palatoquadrate and hyomandibula containing a single gill-like pseudobranch, or create a middle ear cavity, but it never develops into a fully formed gill with two hemibranchs. The belief that a complete spiracular gill must be the ancestral condition led some 20th century researchers to search for such a gill between the mandibular and hyoid arches in early jawed vertebrates. This hypothesized ancestral state was named the aphetohyoidean condition, but so far it has not been verified in any fossil; supposed examples, such as in the acanthodian Acanthodes and symmoriid chondrichthyans, have been reinterpreted and discounted. Here we present the first confirmed example of a complete spiracular gill in any vertebrate, in the galeaspid (jawless stem gnathostome) Shuyu. Comparisons with two other groups of jawless stem gnathostomes, osteostracans and heterostracans, indicate that they also probably possessed full-sized spiracular gills and that this condition may thus be primitive for the gnathostome stem group. This contrasts with the living jawless cyclostomes, in which the mandibular and hyoid arches are strongly modified and the hyomandibular pouch is lost in the adult. While no truly aphetohyoidean spiracular gill has been found in any jawed vertebrate, the recently reported presence in acanthodians of two pseudobranchs suggests a two-step evolutionary process whereby initial miniaturization of the spiracular gill was followed, independently in chondrichthyans and osteichthyans, by the loss of the anterior pseudobranch. On the basis of these findings we present an overview of spiracular evolution among vertebrates.
... This has important implications for the interpretation of the morphologically similar spiracular region in tetrapodomorph fishes (see below). By contrast, the small spiracles of sturgeons and paddlefishes seem to have no respiratory function (Burggren, 1978;Burggren and Bemis, 1991). In neopterygians (gars, bowfins and teleosts) the spiracles are vestigial or absent, although the pseudobranch often persists inside the gill chamber. ...
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About this Research Topic The fish to tetrapod transition transformed the tetrapod body plan, eventually allowing tetrapods to move, eat, breathe, and reproduce on land. Reconstruction of soft tissues in early tetrapods and their relatives has the potential to solve controversies about the behavior and ecology of the earliest terrestrial vertebrates. This task has been attempted many times in many different ways, from detailed drawings made in the 1920s to modern biomechanical models. We aim to present soft tissue descriptions and an overview of current soft tissue reconstruction methods and what they can tell us about functional anatomy in extinct animals. By doing so, we can help to define remaining challenges and project the next advances in this field. We are interested in manuscripts that explore the use of various reconstruction methods and what they can tell us about the evolution of soft tissue anatomy and function surrounding the tetrapod water-land transition. These should include studies using a wide variety of methods, taxa, and anatomical structures. Especially welcome are studies on: • Taxa closely related to stem tetrapods, particularly sarcopterygian fish, stem tetrapods, stem and early amniotes, and stem lissamphibians • Methods grounded in experimental data from extant taxa, such as comparative anatomy, development, and phylogenetic relationships • Paleontological methods such as exceptionally preserved fossils and high-resolution scans • Virtual methods such as biomechanical models • Soft tissue structures such as muscles, cartilage, vessels, and nerves Keywords: Sarcopterygia, fossil, fin-limb, muscle, biomechanics With 13 contributions by 48 authors, incl.: Ryan M. Campbell, Gabriel Vinas, Maciej Henneberg and Rui Diogo; Alice M. Clement, Corinne L. Mensforth, T. J. Challands, Shaun P. Collin and John A. Long; Virginia Abdala, Luciana Cristobal, Mónica C. Solíz and Daniel A. Dos Santos; Nikolay Natchev, Kristina Yordanova, Sebastian Topliceanu, Teodora Koynova, Dimitar Doichev and Dan Cogălniceanu; Michelle Zwafing, Stephan Lautenschlager, Oliver E. Demuth and John A. Nyakatura; Julia Molnar; Tatsuya Hirasawa, Camila Cupello, Paulo M. Brito, Yoshitaka Yabumoto, Sumio Isogai, Masato Hoshino and Kentaro Uesugi; Rohan Mansuit and Anthony Herrel; Ingmar Werneburg and Pascal Abel; Jacob B. Pears, Carley Tillett, Rui Tahara, Hans C. E. Larsson and Catherine A. Boisvert; Pascal Abel, Yannick Pommery, David Paul Ford, Daisuke Koyabu and Ingmar Werneburg; Zhikun Gai, Min Zhu, Per Erik Ahlberg and Philip Donoghue https://www.frontiersin.org/research-topics/14838 https://www.frontiersin.org/research-topics/14838/tetrapod-water-land-transition-reconstructing-soft-tissue-anatomy-and-function#articles
... The species possesses distinctive physiological features such as their electrosensory system (Kistler 1906;Nachtrieb 1906;Russell et al. 1999;Wilkins 2001;Wilkins et al. 2002). Behavioral traits such as ram ventilation (Burggren and Bemis 1992;Sanderson et al. 1994), extensive migrations (Russell 1986;Firehammer and Scarnecchia 2006), and foraging methods (Fredericks 1994;Kozfkay and Scarnecchia 2002) are adaptive to their complex large river environments. ...
Technical Report
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... Studies and observations in the past three decades (Fredericks and Scarnecchia 1997;Scarnecchia et al. 2009; have provided clues about which factors may affect recruitment, and which hypotheses deserve more thorough evaluation. The limited results available support the hypothesis that young Paddlefish, as their high metabolism (higher than sturgeon) and perpetual motion (Burggren and Bemis 1992) would indicate, are in a race to grow large enough and obtain sufficient energy reserves to get through the first winter (in northern latitudes) and to reach a size in all locations where predation rates decrease to low levels. Successful recruitment may depend on how many fish in an annual cohort can grow to a size at which they can escape predation and recruit; i.e., from age-0 (Figure 3), to age-1 or age-2 (Figures 4 and 5). ...
Chapter
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... When the 90˚model was placed in a recirculating flow tank at realistic flow speeds, cross-step filtration occurred at very small intraoral pressures of approximately 11.5 Pa [8]. This filtration system at a low pressure head is consistent with the small intraoral pressures of approximately 13 Pa recorded during ram ventilation in live paddlefish [65] as well as the pressure head of 113 Pa calculated across the filtering apparatus of whale sharks [17]. ...
Article
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Vortical cross-step filtration in suspension-feeding fish has been reported recently as a novel mechanism, distinct from other biological and industrial filtration processes. Although crossflow passing over backward-facing steps generates vortices that can suspend, concentrate, and transport particles, the morphological factors affecting this vortical flow have not been identified previously. In our 3D-printed models of the oral cavity for ram suspension-feeding fish, the angle of the backward-facing step with respect to the model’s dorsal midline affected vortex parameters significantly, including rotational, tangential, and axial speed. These vortices were comparable to those quantified downstream of the backward-facing steps that were formed by the branchial arches of preserved American paddlefish in a recirculating flow tank. Our data indicate that vortices in cross-step filtration have the characteristics of forced vortices, as the flow of water inside the oral cavity provides the external torque required to sustain forced vortices. Additionally, we quantified a new variable for ram suspension feeding termed the fluid exit ratio. This is defined as the ratio of the total open pore area for water leaving the oral cavity via spaces between branchial arches that are not blocked by gill rakers, divided by the total area for water entering through the gape during ram suspension feeding. Our experiments demonstrated that the fluid exit ratio in preserved paddlefish was a significant predictor of the flow speeds that were quantified anterior of the rostrum, at the gape, directly dorsal of the first ceratobranchial, and in the forced vortex generated by the first ceratobranchial. Physical modeling of vortical cross-step filtration offers future opportunities to explore the complex interactions between structural features of the oral cavity, vortex parameters, motile particle behavior, and particle morphology that determine the suspension, concentration, and transport of particles within the oral cavity of ram suspension-feeding fish.
... As a cruising zooplantivore and a ram ventilator (Burggren & Bemis, 1992), paddlefish have white muscle tissue and a considerable amount of red muscle (Decker, Crum, Mims, & Tidwell, 1991;Lou et al., 2000) outside of the white muscle core, next to the integument (D. ...
Article
... For these species, adopting vortex movements may be beneficial because individuals could combine continued motion with energetic savings as a result of swimming in the slipstreams of others (Couzin et al. 2002, Hemelrijk et al. 2015Marras et al. 2015). However, only a very small number of obligate swimmer species are known, such as some sharks (Carlson et al. 2004;Dowd et al. 2006), paddlefish, and tuna (Burggren and Bemis 1992;Wegner et al. 2010). This need to breathe can therefore not explain the adoption of collective vortex movements in many fish species. ...
Article
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Ant mill, caterpillar circle, bat doughnut, amphibian vortex, duck swirl, and fish torus are different names for rotating circular animal formations, where individuals turn around a common center. These “collective vortex behaviors” occur at different group sizes from pairs to several million individuals and have been reported in a large number of organisms, from bacteria to vertebrates, including humans. However, to date, no comprehensive review and synthesis of the literature on vortex behaviors has been conducted. Here, we review the state of the art of the proximate and ultimate causes of vortex behaviors. The ubiquity of this behavioral phenomenon could suggest common causes or fundamental underlying principles across contexts. However, we find that a variety of proximate mechanisms give rise to vortex behaviors. We highlight the potential benefits of collective vortex behaviors to individuals involved in them. For example, in some species, vortices increase feeding efficiency and could give protection against predators. It has also been argued that vortices could improve collective decision-making and information transfer. We highlight gaps in our understanding of these ubiquitous behavioral phenomena and discuss future directions for research in vortex studies.
... Thus, we should see a stronger component of suction feeding in the oarfish than in paddlefish or sardines. Again, observations both of paddlefish and of sardines suggest that this is the case, and both of these species are ram-suspension feeders (Burggren and Bemis 1992), although the data supporting their placement on Fig. 6 is less quantitative than for the elasmobranchs shown. ...
... Thus, we should see a stronger component of suction feeding in the oarfish than in paddlefish or sardines. Again, observations both of paddlefish and of sardines suggest that this is the case, and both of these species are ram-suspension feeders (Burggren and Bemis 1992), although the data supporting their placement on Fig. 6 is less quantitative than for the elasmobranchs shown. ...
Article
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When feeding, most aquatic organisms generate suction that draws prey into the mouth. The papers in this volume are a demonstration of this fact. However, under what circumstances is suction ineffective as a feeding mechanism? Here we consider the interplay between suction, ram, and biting, and analyze the contribution of each to the capture of prey by a wide variety of species of fish. We find, not surprisingly, that ram is the dominant contributor to feeding because suction, and biting, are only effective when very close to the prey. As species utilize more strongly ram-dominated modes of feeding, they may be released from the morphological and behavioral constraints associated with the need to direct a current of water into the head. Morphological and behavioral changes that facilitate larger gapes and stronger jaws are explored here, including predators that lack a protrusile upper jaw, predators with elongate jaws, predators that rely on suspension feeding, and predators that bite. Interestingly, while the mobility of the jaws and the shape of the opening of the mouth are modified in species that have departed from a primary reliance on suction feeding, the anterior-to-posterior wave of expansion persists. This wave may be greatly slowed in ram and biting species, but its retention suggests a fundamental importance to aquatic feeding.
... Thus, we should see a stronger component of suction feeding in the oarfish than in paddlefish or sardines. Again, observations both of paddlefish and of sardines suggest that this is the case, and both of these species are ram-suspension feeders (Burggren and Bemis 1992), although the data supporting their placement on Fig. 6 is less quantitative than for the elasmobranchs shown. ...
Article
Full-text available
When feeding, most aquatic organisms generate suction that draws prey into the mouth. The papers in this volume are a demonstration of this fact. However, under what circumstances is suction ineffective as a feeding mechanism? Here we consider the interplay between suction, ram, and biting, and analyze the contribution of each to the capture of prey by a wide variety of species of fish. We find, not surprisingly, that ram is the dominant contributor to feeding because suction, and biting, are only effective when very close to the prey. As species utilize more strongly ram-dominated modes of feeding, they may be released from the morphological and behavioral constraints associated with the need to direct a current of water into the head. Morphological and behavioral changes that facilitate larger gapes and stronger jaws are explored here, including predators that lack a protrusile upper jaw, predators with elongate jaws, predators that rely on suspension feeding, and predators that bite. Interestingly, while the mobility of the jaws and the shape of the opening of the mouth are modified in species that have departed from a primary reliance on suction feeding, the anterior-to-posterior wave of expansion persists. This wave may be greatly slowed in ram and biting species, but its retention suggests a fundamental importance to aquatic feeding.
... This indicates that restricted gill openings are not ideal for the high levels of activity required for a typical pelagic fish. For example, a small gill opening may not be suitable for fishes such as paddlefishes (Polyodontidae) that rely on ram ventilation (Burggren and Bemis, 1991). Benthic and structure-associated fishes are, to some extent, released from the selective pressures for and morphological constraints of extreme drag reduction and therefore may be more likely to possess modified ventilatory structures such as restricted gill openings. ...
Article
A phylogenetic survey is a powerful approach for investigating the evolutionary history of a morphological characteristic that has evolved numerous times without obvious functional implications. Restricted gill openings, an extreme modification of the branchioste-gal membrane, are an example of such a characteristic. We examine the evolution of branchiostegal membrane morphology and highlight convergent evolution of restricted gill openings. We surveyed specimens from 433 families of actinopterygians for branchiostegal membrane morphology and measured head and body dimensions. We inferred a relaxed molecular clock phylogeny with branch length estimates based on nine nuclear genes sampled from 285 species that include all major lineages of Actinopterygii. We calculated marginal state reconstructions of four branchiostegal membrane conditions and found that restricted gill openings have evolved independently in at least 11 major actinopterygian clades, and the total number of independent origins of the trait is likely much higher. A principal component analysis revealed that fishes with restricted gill openings occupy a larger morphospace, as defined by our linear measurements, than do fishes with nonrestricted openings. We used a decision tree analysis of ecological data to determine if restricted gill openings are linked to certain environments. We found that fishes with restricted gill openings repeatedly occur under a variety of ecological conditions, although they are rare in open-ocean pelagic environments. We also tested seven ratios for their utility in distinguishing between fishes with and without restricted gill openings, and we propose a simple metric for quantifying restricted gill openings (RGO), defined as a ratio of the distance from the ventral midline to the gill opening relative to half the circumference of the head. Functional explanations for this specialized morphology likely differ within each clade, but its repeated evolution indicates a need for a better understanding of diversity of ventilatory morphology among fishes.
... The swimming undulations of the paddlefish trunk impart a lateral oscillating motion to the rostrum, with the cranium acting as the fulcrum. Paddlefishes are ram ventilators (Burggren and Bemis, 1992), so swimming is continuous. This saccade-like motion may serve to enhance prey detection by increasing the width of the electrical scan field. ...
Article
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A comparison is made between a mammalian, monotreme species and an actinopterygian fish that have each, indepen dently, evolved a similar, spoonbill-shaped rostral bill organ whose array of electroreceptors provides sufficient spatial information for prey capture in a freshwater environment without the need for visual cues. The platypus, Ornithorhyn-cus anatinus (Monotremata, Mammalia), has approximately 40,000 electroreceptors arranged in parasagittal rows on the bill organ. By means of behavioral and electrophysiological recording experiments in platypus, it has been shown that this array of electroreceptors can trigger an accurately directed head saccade to intersect aquatic prey that emit elec-trical signals. The threshold field strength for prey detection by platypus signals is 50 microvolts/cm, two orders of magni-tude more sensitive than individual electroreceptors. The pad-dlefish, Polyodon spathula (Osteichthyes, Actinopterygii), can similarly execute a lateral head saccade to intersect prey, with a threshold field strength around 10 microvolts/cm, con-siderably more sensitive than the presumed sensitivity of individual electroreceptors. The remarkable anatomical and behavioral similarities between these two independent elec-troreceptive systems are described and discussed. Major differences between the two bill-organ systems include the mechanism of transduction at the electroreceptors and a prominent cooperative role played by 60,000 mechanorecep-tors that are interdigitated among the electroreceptors in the platypus bill but not in the paddlefish.
... Individual small (18−20 cm) paddlefish were videotaped while capturing Daphnia prey one-by-one, swimming in the viewing chamber of a recirculating stream of water ("swim mill", Fig. 1), located in a closed dark temperature-regulated environmental room [14,18,20,23]. Near-infrared illumination, invisible to these fish [24], was from arrays of lightemitting diodes. ...
Article
Weak electrical noise applied in the water around small paddlefish, Polyodon spathula, increases the spatial range over which they can detect and capture planktonic prey (Daphnia), demonstrating stochastic resonance at the level of an animal's feeding behavior. Here we show that optimal-amplitude (~ 0.5 μ V·cm-1) noise causes a fish to prefer more vertical angles of attack when striking at prey, as revealed in polar graphs. Increased spatial range is also seen in horizontal directions, as outlying shoulders in the probability distribution of horizontal strike distances. High levels of noise increased the distance that approaching prey travelled along the rostrum (an elongated appendage anterior to the head, functioning as an electrosensitive antenna), before the fish first showed a visible fin or body motion in response. There was no significant effect of optimal-amplitude noise on the rate of strikes, although high-amplitude noise reduced the strike rate. The behavioral data were confirmed in neurophysiological experiments demonstrating that stochastic resonance occurs in individual electroreceptors, and in fact occurs at a similar optimal noise level as in behavioral experiments. We conclude that stochastic resonance can be demonstrated in the behavior of animals, and that animals can make use of the increased sensory information available during near-threshold environmental noise.
... In the other approach, oxygen conformers enable a decline in respiration rates as environmental oxygen decreases, with concomitant reductions in metabolic rate and aerobic metabolism [7]. Paddlefish are oxygen regulators and maintain constant respiration rates from 150 mm Hg to 90 mm Hg [8]. Tolerance to hypoxia can be regulated by certain diet components, such as n-3 HUFA [9] and vitamin E [10]. ...
Article
Full-text available
A growth trial was conducted to detect the effects of different diets on the growth performance and hypoxia adaptation capacity of Mississippi Paddlefish (Polyodon spathula) larvae. The larvae were fed with live food, formulated diets, and 1/2 live food with 1/2 formulated diets. After a 15-d growth trial, final body weight and total body length were measured, and five larvae from each dietary group were subjected to 1 h of hypoxia treatment. Serum total antioxidant capacity (T-AOC), serum superoxide dismutase (SOD), and liver malondialdehyde (MDA) were measured. Final body weight and weight gain of the fish fed live food were significantly higher than the values for the other two groups. Total body length of the fish fed live food and 1/2 live food with 1/2 formulated diets exhibited no significant difference. After hypoxia treatment, serum T-AOC and SOD activities of the fish fed formulated diets were significantly lower than those of the other two groups. Liver MDA content of the fish fed with live food was significantly higher than that of the other two groups. In conclusion, larval paddlefish fed with an appropriate proportion of live food and formulated diets exhibit improved adaptive capacity to hypoxia.
... Among extant fishes, spiracles are common in elasmobranchs (sharks and rays) where, in addition to sensory functions, they sustain mouth-bypassing ventilatory flow to the gills when the subterminal mouth is obstructed by substrate or engaged in prey manipulation [2][3][4] . A few extant early-diverging actinopterygian lineages (Polypteriformes (bichirs and ropefish) and Acipenseriformes (sturgeons and paddlefish)) have spiracles, but only the polypterids, a freshwater African family (B11 species of Polypterus and the monotypic Erpetoichthys) have spiracles large enough to significantly aid in respiration [4][5][6][7] . ...
Article
Full-text available
The polypterids (bichirs and ropefish) are extant basal actinopterygian (ray-finned) fishes that breathe air and share similarities with extant lobe-finned sarcopterygians (lungfishes and tetrapods) in lung structure. They are also similar to some fossil sarcopterygians, including stem tetrapods, in having large paired openings (spiracles) on top of their head. The role of spiracles in polypterid respiration has been unclear, with early reports suggesting that polypterids could inhale air through the spiracles, while later reports have largely dismissed such observations. Here we resolve the 100-year-old mystery by presenting structural, behavioural, video, kinematic and pressure data that show spiracle-mediated aspiration accounts for up to 93% of all air breaths in four species of Polypterus. Similarity in the size and position of polypterid spiracles with those of some stem tetrapods suggests that spiracular air breathing may have been an important respiratory strategy during the fish-tetrapod transition from water to land.
... The combination of a relatively small peduncle with a deep narrow caudal fin, called " narrow necking , " minimizes side forces in swimming that would otherwise make the head of a fish oscillate laterally, while generating and maintaining substantial thrust. This enables paddlefish to swim efficiently in a straight line, facilitating ram-ventilation and filterfeeding (Burggren and Bemis 1992; Sanderson et al. 1994). Significant differences among the series in the size of the caudal lobes result in apparent differences in the caudal aspect ratio, the ratio of span (distance measured between upper and lower tips of the caudal fin) to chord (distance measured from peduncle to edge of caudal fin). ...
Article
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Paddlefish rostra vary in size and shape suggesting existence of multiple morphotypes. Measurements for 118 adult paddlefish from a Mississippi delta river indicate that the rostrum becomes shorter, narrower, and straighter as a fish grows. Negative allometric growth of rostra, and high variation within size classes, may obscure existence of distinctive rostral morphotypes.
... Many fishes are able to buccal pump when needed but switch to ram ventilation at appropriate swimming speeds. Facultative ram ventilation has been documented in paddlefish Polyodon spathula (Burggren and Bemis, 1992;Sanderson et al., 1994), sandtiger sharks Odontaspis (¼ Eugomphodus or Carcharias) taurus (von Wahlert, 1964), leopard sharks Triakis semifasciata (Hughes 1960b), a variety of salmonids (Roberts, 1978;SteVensen, 1985), several pelagic species such as mackerel Scomber scombrus, blue runner Caranx crysos, bluefish Pomatomus saltatrix, scup Stenotomus crysops, and the halfmoon Medialuna californica (Roberts, 1975), and sharksuckers Echeneis naucrates and remoras Remora remora when attached to a fast-swimming shark or aquatic mammal (Muir and Buckley, 1967;SteVensen and Lomholt, 1983;SteVensen, 1985). Interestingly, a number of species, including some that routinely move into open water habitats, never switch to ram ventilation. ...
Article
To facilitate oxygen uptake and carbon dioxide excretion, fishes ventilate their gas exchange surfaces with water or air. Because water and air differ substantially in their density, viscosity, and oxygen content, the biomechanical problems associated with aquatic and aerial ventilation also differ. Nonetheless, aerial and aquatic respiratory pumps do share one biomechanical challenge stemming from the fact that muscles only generate force in the direction of shortening. It is a simple matter for muscle contraction to generate positive pressure and force fluid out of a cavity, but respiratory pumps also require an expansive phase to refill the cavity with new fluid. Some biomechanical trickery is necessary for muscle shortening to cause the expansion of a cavity and the generation of subambient pressure. This trickery generally takes the form of a lever system or occasionally elastic recoil. The primary biomechanical problems in the design of aquatic respiratory pumps stem from the physical and chemical properties of water: high density, high viscosity, and low oxygen content. The biomechanical challenges for aerial respiratory pumps stem from predation risk, hydrostatic pressure, buoyancy, surface tension, and mechanical conflicts between breathing and feeding.
... It is also known that American paddlefish swim in a fairly primitive manner involving undulation of nearly the entire body (Wills, 1993). (Burggren and Bemis, 1992; Wills, 1993) ...
... The combination of a relatively small peduncle with a deep narrow caudal fin, called " narrow necking , " minimizes side forces in swimming that would otherwise make the head of a fish oscillate laterally, while generating and maintaining substantial thrust. This enables paddlefish to swim efficiently in a straight line, facilitating ram-ventilation and filterfeeding (Burggren and Bemis 1992; Sanderson et al. 1994). Significant differences among the series in the size of the caudal lobes result in apparent differences in the caudal aspect ratio, the ratio of span (distance measured between upper and lower tips of the caudal fin) to chord (distance measured from peduncle to edge of caudal fin). ...
Chapter
Full-text available
... Juvenile sablefish were less affected by food distribution, as individuals receiving clumped food swam faster than fish receiving dispersed food only during the first hour of foraging. Data for a variety of fish species indicate that energy consumption is nonlinearly related to swimming speed, such that it costs lsproportionately more to swim faster (Tytler 1969, Puckett & Dill 1984, Bernatchez & Dodson 1985, Dabrowski 1986, Furnell 1987, Bushnell & Brill 1991, Burggren & Bemis 1992). As a result, we conclude that juvenile walleye pollock foraging for clumped food expended more energy than dispersed food foragers. ...
Article
Prior studies have demonstrated that juvenile walleye pollock Theragra cl?alcogramma forage socially in schools for spatially and temporally clumped food, but forage more independently for spatially and temporally dispersed food. One advantage of social foraging is that fish in schools may be able to locate more food clumps than fish foraging individually. However, data also indicate that wall-eye pollock swim faster when foraging socially. CVe conducted laboratory experiments to evaluate the effect of food distribution upon the energetic foraglng costs lncurred by juvenile walleye pollock and sablefish Anaplopoma fimbna. We predicted that when given identical rations, fish receiving clumped food would swim faster, expending more energy, and therefore grow more slowly than fish receiving dispersed food After 2 wk under these 2 foraging regimes, juvenile walleye pollock receiving clumped food swam 50% faster, but experienced 19% lower growth, than walleye pollock receiving dispersed food. Sablefish demonstrated only a weak swim speed response, with no difference in growth between food distributions. Our results demonstrate that although social foraging may increase encounter rates with food, in some specles there may also be an energetic cost for this behavior, which will have a n influence upon energet~c efficiency, potentially affecting growth and survival.
... Polyodon depends on ram ventilation, as evidenced by the absence of a buccal valve and the inability to completely close either the opercular chamber or the mouth. As further evidence of the critical role of ram ventilation, Burggren & Bemis (1992) found that juvenile paddlefishes are nearly as aerobic as cruising bluefin tuna, Thunnus thunnus. Speculating on the connection between ram ventilation and the evolution of filter feeding within Polyodontidae, they linked the potential to evolve filter feeding to the prior evolution of ram ventilation. ...
Chapter
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Acipenseriformes occupy a special place in the history of ideas concerning fish evolution, but in many respects, phylogenetic studies of the group remain in their infancy. Even such basic questions as the monophyly of Acipenser (the largest genus) are unanswered. We define relationships based on comparative osteology, which allows us to incorporate well-preserved fossils into analyses. Acipenseriformes has existed at least since the Lower Jurassic (approximately 200 MYBP), and all fossil and recent taxa are from the Holarctic. Phylogenetic relationships among Paleozoic and Early Mesozoic actinopterygians are problematic, but most workers agree that Acipenseriformes is monophyletic and derived from some component of ‘paleonisciform’ fishes. (‘Paleonisciformes’ is a grade of primitive non-neopterygian actinopterygians, sensu Gardiner 1993.) Taxa discussed in comparison here are: †Cheirolepis, Polypterus, †Mimia. †Moythomasia, †Birgeria, †Saurichthys, Lepisosteus and Amia. We review generic diversity within the four nominal families of fossil and recent Acipenseriformes (†Chondrosteidae, †Peipiaosteidae, Polyodontidae, and Acipenseridae), and provide a cladogram summarizing osteological characters for those four groups. Monophyly of the two extant families is well-supported, but there are no comprehensive studies of all of the known species and specimens of †Chondrosteidae and †Peipiaosteidae. As a result, sister-group relationships among †Chondrosteidae, †Peipiaosteidae, and Acipenseroidei (= Polyodontidae + Acipenseridae)are unresolved. We discuss five features fundamental to the biology of acipenseriforms that benefit from the availability of our new phylogenetic hypothesis: (1) specializations of jaws and operculum relevant to jaw protrusion, feeding, and ram ventilation; (2) anadromy or potamodromy and demersal spawning; (3) paedomorphosis and evolution of the group; (4) the biogeography of Asian and North American polyodontids and scaphirhynchines; and (5) the great abundance of electroreceptive organs in the rostral and opercular regions. Finally, we summarize our nomenclatural recommendations.
... Remarkably, juvenile paddlefish can detect and capture plankton at distances up to 90mm from the surface of the rostrum . The larger paddlefish that are filter feeders may use electroreception to identify larger concentrations of zooplankton or to determine when to switch from ram ventilation (Burggren and Bemis, 1992) to the faster swimming speed that they appear to use during ram suspension feeding (Sanderson et al. 1994). However, there is no evidence of selective behaviour for filter feeding on particular types of zooplankton, because their gut contents contain the same complement of the appropriate sized species that are present in their environment (Michaletz et al. 1982). ...
... It is unclear whether this disparity arises from morphological differences or differences in how the flow through the respiratory tract was modeled. However, the pressure head of 113 Pa calculated for whale sharks is consistent with the pressure observed across fish gills during routine ventilation, which falls between 30 and 200 Pa for a diverse range of taxa (Hughes, 1960a,b; Burggren and Bemis, 1992;Ferry-Graham, 1999). Several workers have questioned the effectiveness of the whale shark's filtering pads at sustaining a high flow of water through them during ram filter feeding ( Taylor et al., 1983;Sanderson and Wassersug, 1993) and their ability to filter out plankton smaller than the holes in the filtering pads ( Clark and Nelson, 1997). ...
Chapter
The foremost function of a gas exchanger is to obtain O2 from the external milieu and discharge CO2 into the same (e.g., Dejours 1988; Weibel 1984). Of the three natural states of matter, i.e., solid, liquid, and gas, it is only the fluid state (liquid and gas) that is physically, i.e., atomically/molecularly configured to contain and transmit the respiratory gases, O2 and CO2. At physiological range of temperature, water and air are the only two naturally occurring respirable fluids.
Chapter
The biological aspects of a fish, paddlefish in particular, are important to the understanding of form and functional relationships, how the environment and habitat have affected natural distribution, how anthropogenic perturbations and exploitation have affected the current status of populations, and the need to culture paddlefish. This chapter presents a taxonomic summary condensed from Georgi and Dingerkus. The American paddlefish and the Chinese paddlefish are the only two extant species of the family and these are geographically separated. Paddlefish are long-lived and may reach more than 2 m in length and 70 kg. The most noticeable anatomical feature is the unique spatulate rostrum that extends up to one-third of its body length. The chapter describes the skeletal system of paddlefish. The postembryonic gonadal differentiation, as well as sexual maturity of paddlefish occur at a larger size and older age compared to many other fishes.
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We re-define the Cretaceous bony fish genus Rhinconichthys by re-describing the type species, R. taylori, and defining two new species, R. purgatorensis sp. nov. from the lowermost Carlile Shale (middle Turonian), southeastern Colorado, United States; and R. uyenoi sp. nov. from the Upper Cretaceous (Cenomanian) Mikasa Formation, Middle Yezo Group, Hokkaido, Japan. Rhinconichthys purgatoirensis sp. nov. is designated on a newly discovered specimen consisting of a nearly complete skull with pectoral elements. Only known previously by two Cenomanian age specimens from England and Japan, the North American specimen significantly extends the geographic and stratigraphic range of Rhinconichthys. The skull of Rhinconichthys is elongate, including an expansive gill basket, and estimated maximum body length ranges between 2.0 and 2.7 m. Rhinconichthys was likely an obligate suspension-feeder due to its derived cranial morphology, characterized by a remarkably large and elongate hyomandibula. The hyomandibula mechanically acts as a lever to thrust the jaw articulation and hyoid arch both ventrally and anterolaterally during protraction, thus creating a massive buccal space to maximize filtering of planktonic prey items. Cladistic analysis supports a monophyly of suspension-feeding pachycormids including Rhinconichthys, but further resolution within this clade will require more information through additional fossil specimens.
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The paddlefish paddle and its clusters of ampullary organs represent a novel evolutionary adaptation of the passive electrosense for zooplanktivorous feeding. The rostrum serves as an antenna extended in front of the fish to detect plankton encountered during continuous, ram-ventilating swimming. With itc exten- sive population of highly sensitive ampullary electroreceptors, the paddlefish is ideally suited to utilize the rich planktonic resource, a diet of near microscopic organisms otherwise difficult to detect by visual predators in the turbid waters of the Mississippi River drainage. The zooplankton, primarily cladocerans, e.g., Daphnia, exhibit dipole DC and oscillating electric field potentials that are readily detected by the paddlefish. These environmental signals are transduced into neuronal responses in the primary afferent fibers of the anterior lateral line nerve. Each afferent fiber branches to innervate multiple ampullae within the peripheral clusters. The afferents terminate in the specialized electrosensory lobes of the hindbrain medulla, the large dorsal octavolateralis nuclei (DON). Electrosensory information is passed on to large pyramidal-like neurons in the DON that project robustly via brainstem tracts into the midbrain innervat- ing the tectum mesencephalicus, the lateral mesencephalic nucleus, and the torus semicircularis. Electrosensory processing in the DON also involves descending input from both midbrain and cerebellar nuclei, in addition to commissural feedback from thecontralateral DON. Direct innervation of the tectum from the DON is unique to the paddlefish and may reflect dominance of the electrosensory system in tectal orientation, a mechanism essential for prey localization and capture.
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Abedus herberti is an aquatic bug that carries a subalar store of atmospheric air for use during submersion. When submersed, adult bugs routinely show two patterns of behaviour we call gaping and dynamic gaping. We studied these behaviours to determine when they are expressed and tested the hypothesis that the behaviours serve a respiratory function. Gaping and dynamic gaping occurred when bugs were positioned sufficiently deep in water that they could not refresh air stores without releasing their hold on the substrate and floating to the surface. Gaping and dynamic gaping occurred more frequently as water depth increased, and bugs performing these behaviours remained submersed longer than bugs that did not express these behaviours. Bugs permitted to express gaping and dynamic gaping remain submersed longer than bugs that were experimentally prevented from performing the behaviours. Bugs also remained submersed longer in high oxygen water than in low oxygen water. We conclude that gaping allows the subalar air store to function as a physical gill and that dynamic gaping is a form of behavioural ventilation. Adult A. herberti are buoyant and must swim or hold onto a substrate to remain submersed. Extending submersion time increases predatory efficiency, reduces the frequency of surfacing, saves energy and reduces predation risk.
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