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Introduction
As a integrative physiologist, I believe that it is important to articulate the power of comparative and evolutionary physiology and to point out that these approaches are not mutually exclusive to biomedical sciences.
Comparative physiology, at its most basic level, seeks to discover how animals work, and, most importantly, why animals work the way they do. These two seemingly straightforward questions have far-reaching implications and require a variety of investigative approaches.
Additional affiliations
January 1986 - December 1987
October 1984 - December 1985
January 1988 - June 1992
Education
June 1979 - October 1984
Publications
Publications (196)
Vertebrates utilize various respiratory organs like gills, lungs, and skin in combination with diverse cardiovascular structures, including single, three, and four-chambered hearts, to enable oxygen delivery and carbon dioxide removal. They also exhibit differences in aerobic and anaerobic metabolism during exertion, but the cardiorespiratory gas t...
Blood-based biomarkers of brain injury may be useful for monitoring brain health in athletes at risk for concussions. Two putative biomarkers of sport-related concussion, neurofilament light (NfL), an axonal structural protein, and S100 calcium-binding protein beta (S100B), an astrocyte-derived protein, were measured in saliva, a biofluid which can...
For well over 150 years, factors of safety (also known as safety factors) have been a fundamental engineering concept that expresses how much stronger a system is compared with the intended load. The pioneering work of Robert McNeill Alexander in the early 1980s applied this engineering concept to biomechanics. Over the next decade, evidence from c...
The global medical community has exalted the vaccine as the champion solution to end the violent toll inflicted by COVID-19. While the role of vaccines cannot be undervalued in wide-scale intervention, presenting them as the sole solution exonerates individuals of the importance of taking ownership over their lifestyle choices. This editorial focus...
This study sought to describe head impact exposure in women’s collegiate club lacrosse. Eleven women’s collegiate club lacrosse players wore head impact sensors during eight intercollegiate competitions. Video recordings of competitions were used to verify impact data. Athletes completed questionnaires detailing their concussion history and perceiv...
Elevations of metabolic rate, for example during physical activity, elicit immediate and coordinated respiratory and cardiovascular responses that ensure adequate diffusive and convective fluxes of O2 from the environment (water or air) to the mitochondria where ATP is produced. The same physiological responses also provide for CO2 to be removed in...
Exposure to head impacts is common in soccer and, in some cases, has been associated with neurocognitive and physiological consequences in soccer players. Ball-to-head impacts are particularly frequent, as soccer players regularly use their heads to pass, clear, and shoot the ball during game play and practice. The attenuation of head accelerations...
A growing body of evidence suggests that chronic, sport-related head impact exposure can impair brain functional integration and brain structure and function. Evidence of a robust inverse relationship between the frequency and magnitude of repeated head impacts and disturbed brain network function is needed to strengthen an argument for causality....
Objectives
Recent reports have demonstrated a risk of concussion and subconcussive head impacts in collegiate varsity and international elite water polo. We sought to characterize patterns of head impact exposure at the collegiate club level of water polo.
Design
Prospective cohort study.
Method
Head impact sensors (SIM-G, Triax Technologies) wer...
The SIM-G is a waterproof head impact sensor that has been previously evaluated for use in a headband, but not yet in a mode of attachment suitable for water polo. For this study, a CADEX linear impactor was used to impact a Hybrid III headform while wearing either a headband or modified water polo cap, each housing a SIM-G. In both headgears, the...
Heart rate variability (HRV) provides insight into cardiovascular health and autonomic function. Electrocardiography (ECG) provides gold standard HRV measurements but is inconvenient for continuous acquisition when monitored from the extremities. Optical techniques such as photoplethysmography (PPG), often found in health and wellness trackers for...
The effects of the embryonic environment on juvenile phenotypes are widely recognized. We investigated the effect of embryonic hypoxia on the cardiovascular phenotype of 4-year-old American alligators (Alligator mississippiensis). We hypothesized that embryonic 10% oxygen preconditions cardiac function, decreasing the reduction in cardiac contracti...
Monitor lizards are unique among ectothermic reptiles in that they have high aerobic capacity and distinctive cardiovascular physiology resembling that of endothermic mammals. Here, we sequence the genome of the Komodo dragon Varanus komodoensis, the largest extant monitor lizard, and generate a high-resolution de novo chromosome-assigned genome as...
Recent reports have demonstrated that there is a serious risk of head impact and injury in water polo. The use of protective headgear in contact sports is a commonly accepted strategy for reducing the risk of head injury, but there are few available protective headgears for use in water polo. Many of those that are available are banned by the sport...
Water polo is a contact sport that is gaining popularity in the United States and carries a risk of repeated head impacts and concussion. The frequency and magnitude of sport-related head impacts have not been described for water polo. We aimed to compare patterns of empirically measured head impact exposure of male collegiate water polo players to...
The anatomy of the heart and the respiratory organs differs enormously amongst vertebrates, and the absolute rates of oxygen uptake – both at rest and exercise — are several-fold higher in the endothermic birds and mammals when compared to fish, amphibians and reptiles (all ectothermic). Despite these large differences, all vertebrates can elevate...
Monitor lizards are unique among ectothermic reptiles in that they have a high aerobic capacity and distinctive cardiovascular physiology which resembles that of endothermic mammals. We have sequenced the genome of the Komodo dragon (Varanus komodoensis), the largest extant monitor lizard, and present a high resolution de novo chromosome-assigned g...
Objectives
Return-to-play protocols could be improved by a better understanding of the physiologic effects of mild traumatic brain injury (mTBI). Autonomic dysregulation is thought to underlie many of the multi-dimensional symptoms following mTBI and may derive from altered connectivity in the brain central autonomic network (CAN). Understanding th...
Aquatic animals are known to be sensitive to low oxygen environments. Aquatic hypoxia can limit an animal's capacity for aerobic metabolism, reducing its ability for locomotion, growth, reproduction, and survival. It is thus important for a fish to be able to detect and avoid hypoxic environments or develop an auxiliary method for obtaining oxygen,...
The Commentary by Pörtner, Bock and Mark (Pörtner et al., 2017) elaborates on the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis. Journal of Experimental Biology Commentaries allow for personal and controversial views, yet the journal also mandates that ‘opinion and fact must be clearly distinguishable’ (http://jeb.biologists.org...
African house snakes (Lamprophis fuliginosus) were used to compare the metabolic increments associated with reproduction, digestion, and activity both individually and when combined simultaneously. Rates of oxygen consumption () and carbon dioxide production () were measured in adult female (nonreproductive and reproductive) and adult male snakes d...
By virtue of their cardiovascular anatomy, reptiles and amphibians can shunt blood away from the pulmonary or systemic circuits, but the functional role of this characteristic trait remains unclear. It has been suggested that right-to-left (R-L) shunt (recirculation of systemic blood within the body) fuels the gastric mucosa with acidified and CO2-...
Mammals and birds maintain high arterial partial pressure of oxygen (P O2) values in order to preserve near complete hemoglobin (Hb) oxygen (O2) saturation. In diving mammals and birds, arterial O2 follows a primarily monotonic decline and then recovery quickly after dives. In laboratory studies of submerged freshwater turtles, arterial O2 depletio...
Purpose
Water polo is a sport with a high degree of physicality and aggressive play. Unlike most contact sports, epidemiological data on the incidence or prevalence of head trauma in water polo have not been gathered, reported, or made publicly available. The purpose of this study was to begin a systematic characterization of the risks of head impa...
The notion that bimodal breathers (animals that breathe both air and water) obtain O 2 from the air and exhale CO‐ 2 into the water has been well established in the literature. However, while the majority of supporting experiments tested animals maintained in hypoxic water, freshwater systems that bimodal breather inhabit have been reported to be h...
Mammals and birds maintain a narrow range of arterial P O2 values to preserve near complete O 2 saturation. Since arterial blood gases in mammals and birds are tightly coupled with lung gas values, this is accomplished through changes in ventilation. In reptiles, pulmonary and system circulations are not completely separated and thus, cardiac shunt...
Snakes exhibit large factorial increments in oxygen consumption during digestion, and physical activity, and long-lasting sub-maximal increments during reproduction. Under natural conditions, all three physiological states may occur simultaneously, but the integrated response is not well understood. Adult male and female Checkered Gartersnakes (Tha...
Acute and chronic changes in ambient temperature alter several aspects of reptilian physiology. We investigated the effects of each type of temperature change on reptilian cardiovascular regulation in red-eared slider turtles (Trachemys scripta), a species known to experience marked seasonal changes in ambient temperature. Turtles were instrumented...
Interspecific allometric analyses indicate that mean arterial blood pressure (MAP) increases with body mass of snakes and mammals. In snakes, MAP increases in proportion to the increased distance between the heart and the head, when the heart-head vertical distance is expressed a ρgh, and the rise in MAP is associated with larger heart to normalize...
Freshwater turtles are capable of remaining underwater for over four months. This is in part due to their ability to reduce their metabolism in order to survive long periods of anoxia. Another unique ability freshwater turtles possess is the ability to shunt blood, or cause blood to deviate from the normal cardiovascular circuit due to pulmonary an...
Atropine sulfate is a common anticholingeric drug that is used in human medicine and veterinary medicine, as well as in scientific research. At doses less than 0.1mg/kg, it is used to treat bradycardia, ptyalism, and as an antidote for organophosphate poisoning. Although the effects of atropine have not been thoroughly examined in reptiles, previou...
Physiological cardiac hypertrophy is characterized by reversible enlargement of cardiomyocytes and changes in chamber architecture, which increase stroke volume and VO2 max via augmented convective oxygen transport. Cardiac hypertrophy is known to occur in response to repeated elevations of O2 demand and/or reduced O2 supply in several species of v...
The inaugural Kjell Johansen lecture in the Zoophysiology Department of Aarhus University (Aarhus, Denmark), afforded the opportunity for a focused workshop comprising comparative cardiovascular physiologists to ponder some of the key unanswered questions in the field. Discussions were centered around three themes. The first considered function of...
This study utilized computed spirometry to compare the pulmonary function of two stranded olive ridley sea turtles (Lepidochelys olivacea) presenting with a positive buoyancy disorder with two healthy captive olive ridley sea turtles held in a large public aquarium. Pulmonary function test (PFT) measurements demonstrated that the metabolic cost of...
The objective of this study was to understand the physiological response of red‐eared sliders to investigator presence during routine activities. We measured heart rate continuously in red‐eared sliders during undisturbed and disturbed activities. EKG leads were implanted through the carapace above and below the heart and then attached to a self‐co...
The ancestral in‐parallel circulation of tetrapods combines a single ventricle and two systemic aortae, which allow central vascular shunting. Loss of the shunt and evolution of the in‐series circulatory design, as exemplified by extant mammals and birds, involved independent acquisition of two anatomic features: a complete interventricular septum,...
Burmese pythons ( Python molurus ) and American alligators ( Alligator mississippiensis ) utilize intermittent feeding strategies, with prolonged fasts punctuated by bouts of voracious feeding. Both species exhibit large increases in postprandial oxygen consumption (V̇O 2 ). Presumably in response to increased O 2 demand, P. molurus has been shown...
The goal of this research was to measure oxygen consumption (i.e. VO2) associated with exhaustive activity, digestion, and gravidity in the viviparous Checkered Garter Snake. To determine gravidity, female snakes were imaged with a portable ultrasound. Gas analysis was performed using flow through respirometry with carbon dioxide and oxygen sensors...
The anatomy of the nonavian reptile heart allows for mixing of oxygen rich and oxygen poor blood (cardiac shunts). The degree and the direction of the cardiac shunts are under autonomic control and changes characteristically during the intermittent ventilation of the lungs. While cardiac shunts are detrimental to oxygen transport in the endothermic...
Longitudinal growth rate (LGR) has been shown to correlate with calcified cartilage column height (CCC) in the growth plates of birds. In order to infer limb bone growth patterns in non‐avian dinosaurs, this correlation needs to be documented in crocodilians. We tested the LGR‐CCC correlation in femora of juvenile alligators raised for two years un...
Oxygen levels have fluctuated between 16% and 36% as shown from burial rates of organic carbon over the past 500 million years (my). This cyclical pattern has been associated with animal extinction and implicated as a driving force for physiological adaptation. We use Alligator mississippiensis ( A.M.) as a model species of longevity and adaptabili...
The energetic cost of reproduction in the oviparous snake, Lamprophis fuliginosus (African Brown House Snake) was compared to other elevated metabolic states, specifically exhaustive activity and digestion. To determine gravidity, female snakes were imaged with a portable ultrasound (CTS‐3300, SIUI America, Inc.). Oxygen consumption was determined...
Microanatomy and cross sectional geometry of limb bones are often used to infer life history and locomotor ability of fossil vertebrates based on study of their extant relatives; often the extreme variations in atmospheric oxygen that occurred over geologic time (oxygen levels 30% or more during the Permian, 15% in the Triassic) are not considered....
The cardiovascular (CV) system is the first operational organ system, and reptiles represent evolutionary intermediates between water‐breathing vertebrates and birds and mammals. Reptile eggs are subject to environmental stressors during development, including hypoxia, and we have shown that hypoxia impacts reptilian CV function and maturation. Usi...
The adult phenotype of an organism is the result of its genotype, the environment, and the interaction between the two. Assessing the relative contribution of these factors to the final adult phenotype continues to occupy researchers. Studies have shown clutch effects early in development but few have investigated the persistence of clutch effects...
Hypoxia is a naturally occurring environmental challenge for embryonic reptiles, and this is the first study to investigate the impact of chronic hypoxia on the in ovo development of autonomic cardiovascular regulation and circulating catecholamine levels in a reptile. We measured heart rate (f(H)) and chorioallantoic arterial blood pressure (MAP)...
Hypoxia is a naturally occurring environmental challenge for embryonic non-avian reptiles, and this study is the first to investigate the impact of chronic hypoxia on a possible chemoreflex loop in a developing non-avian reptile. We measured heart rate and blood pressure in normoxic and hypoxic-incubated (10% O(2)) American alligator embryos (Allig...
Over a decade has passed since Powell et al. (Respir Physiol 112:123-134, 1998) described and defined the time domains of the hypoxic ventilatory response (HVR) in adult mammals. These time domains, however, have yet to receive much attention in other vertebrate groups. The initial, acute HVR of fish, amphibians and reptiles serves to minimize the...
Abstract In a previous paper comparing 155 species of snakes, we showed that the position of the heart relative to the head is statistically related to both habitat usage and phylogenetic position ("Phylogeny, ecology, and heart position in snakes," Physiological and Biochemical Zoology 83:43-54). More specifically, we found that, on average, arbor...
Angiotensin II (Ang II) is an important regulator of cardiovascular function in adult vertebrates. Although its role in regulating the adult system has been extensively investigated, the cardiovascular response to Ang II in embryonic vertebrates is relatively unknown. We investigated the potential of Ang II as a regulator of cardiovascular function...
All embryonic and fetal amniotes possess a ductus(i) arteriosus(i) that allows blood to bypass the pulmonary circulation and the non-functional lungs. The central hemodynamic of embryonic reptiles are unique, given the additional systemic aorta that allows pulmonary circulatory bypass, the left aorta (LAo). The LAo exits in the right ventricle or ‘...
The functional and possible adaptive significance of non-avian reptiles' dual aortic arch system and the ability of all non-avian reptiles to perform central vascular cardiac shunts have been of great interest to comparative physiologists. The unique cardiac anatomy of crocodilians - a four-chambered heart with the dual aortic arch system - allows...
Despite having a similar four‐chambered heart, crocodilians and birds differ widely in their aerobic capacity. We investigated whether this is due to differences in outflow tract design, which allows for cardiac shunting in crocodilians, but not in birds. We hypothesized that removal of cardiac shunt will improve aerobic capacity (VO 2 max) by forc...
During vertebrate evolution, atmospheric oxygen (O 2 ) level may have varied from as low as 12% to as high as 30%, but no studies to date have considered the effect of ambient O 2 on skeletal plasticity. We incubated eggs and subsequently grew alligator hatchlings under chronic hypoxia (12% O 2 ), normoxia (21% O 2 ) and hyperoxia (30% O 2 ). Anima...
In contrast to mammals and birds, effects of exercise on bone microstructure in reptiles have received scant attention. We investigated the effects of long‐term exercise on a treadmill or in a flume on limb bones of the American alligator. Juvenile alligators were run or swum to exhaustion every other day for 17 months, and received fluorescent dye...
The vertebrate cardiovascular (CV) system becomes operational early in development and must function and mature both anatomically and physiologically. Deviations in developmental environment create challenges that impact CV function and maturation. Reptilian embryos may be particularly impacted given features of development in egg‐laying species, s...
Introduction Air-breathing vertebrates constitute a large group of diverse animals belonging to different taxonomic classes. Air breathing evolved independently in different groups of fish and early tetrapods, and extant species employ an array of different air-breathing organs that are derived from various existing structures, such as the gastroin...
The cardiovascular system of all animals is affected by gravitational pressure gradients, the intensity of which varies according to organismic features, behavior, and habitat occupied. A previous nonphylogenetic analysis of heart position in snakes-which often assume vertical postures-found the heart located 15%-25% of total body length from the h...
Crocodilians have complete anatomical separation between the ventricles, similar to birds and mammals, but retain the dual aortic arch system found in all non-avian reptiles. This cardiac anatomy allows surgical modification that prevents right-to-left (R-L) cardiac shunt. A R-L shunt is a bypass of the pulmonary circulation and recirculation of ox...
The oxygen transport system in mammals is extensively remodelled in response to repeated bouts of activity, but many reptiles appear to be 'metabolically inflexible' in response to exercise training. A recent report showed that estuarine crocodiles (Crocodylus porosus) increase their maximum metabolic rate in response to exhaustive treadmill traini...
Recent palaeoatmospheric models suggest large-scale fluctuations in ambient oxygen level over the past 550 million years. To better understand how global hypoxia and hyperoxia might have affected the growth and physiology of contemporary vertebrates, we incubated eggs and raised hatchlings of the American alligator. Crocodilians are one of few vert...
Exercise affects the vertebrate skeleton via biomechanical and biochemical stress. Exercise‐induced strains can elicit increased primary bone formation and/or secondary remodelling of limb bones. Exhaustive exercise results in high lactic acid loads, which may require buffering by bone mineral and thus influence bone remodelling. Cardiac shunting i...
Skeletal growth reflects whole‐body growth of the animal, and features of bone microstructure (vascular density, collagen arrangement) can be used to infer an animal's growth strategy. This relationship, however, may be altered by environmental change. Vertebrates are known to have endured large‐scale fluctuations in atmospheric %O 2 during their e...
The breathing pattern of many different air-breathing vertebrates, including lungfish, anuran amphibians, turtles, crocodiles and snakes, is characterized by brief periods of lung ventilation interspersed among apnoeas of variable duration. These intermittent ventilatory cycles are associated with characteristic increases in pulmonary blood flow an...
Reptilian cardiac shunting is hypothesized to confer a fitness advantage via physiological functions including inducing hypometabolism, aiding recovery from metabolic acidosis and facilitating digestion. Elimination of cardiac shunt has n