Elska B. Kaczmarek

My research program seeks to understand the origin and diversification of air breathing in fishes by integrating morphology, physiology, kinematics, function, and ecology within an evolutionary context. The evolution of air breathing was an exceptional innovation among bony fishes that unlocked new regions of ecological space, both on land and in the water. Despite its importance to vertebrate diversity, there are long-standing questions about the early evolution, functional roles, and diversification of air breathing. My research seeks to both shed light onto this great evolutionary transformation and address fundamental questions about the relationships between form and function and the drivers of their diversity.

Many infants are bottle-fed rather than breastfed for a variety of reasons. However, infants use different biomechanics when bottle-feeding compared to breastfeeding and derive greater physiological benefits from breastfeeding. One possible cause of these differences is structural design. Typical bottle nipples have open space inside them, like cow teats, while most mammalian breast tissue has narrow ducts. How does bottle nipple morphology impact suckling mechanics? Using pigs as an animal model, I am using XROMM, electromyography, and intraoral pressure to evaluate how feeding biomechanics and physiology differs between infants raised on biomimetic ducted nipples and those raised on conventional cisternic nipples.

Although lungs and respiratory gas bladders function as organs for both supplying oxygen and buoyancy, air breathing has almost exclusively been studied in the context of hypoxia. How do air breathing fish regulate buoyancy? Do they modify the size, frequency, or type of their air breaths? These questions had only been addressed in one species, bowfin (Hedrick and Jones, 1993). My research showed that royal knifefish, like bowfin, obtain oxygen using the four-stroke breath (the ancestral breath type of actinopterygian fishes) and increase buoyancy using an inspiration-first breath. Inspiration-first breaths have only been described in these two species, and my research on knifefish highlights the possibility that scientists have failed to observe inspiration-first breaths in other air-breathing fishes because they have solely manipulated oxygen availability, not buoyancy.

The X-ray Reconstruction of Moving Morphology (XROMM) workflow enables precise and accurate measurement of the 3D skeletal kinematics underlying animal behaviors. The dynamic endocast method built upon that workflow to measure the rate of volume change within a bounded region of interest. This method has been used to measure oropharyngeal cavity volume (and calculate power) during suction feeding in fishes, oral cavity volume during food processing in macaques, and tidal volume during lung ventilation in sea turtles. We are measuring the precision and accuracy of the dynamic endocast method, using a fish oropharyngeal cavity as a case study.

Macrostomatan snakes are able to swallow enormous prey because of their extensible soft tissues and highly kinetic cranial skeletons. Prior research has hypothesized about how snake cranial bones move during macrostomy, however, in vivo kinematics have not been measured. How do pythons move their bones in order to engulf large prey? How do their cranial morphology and mobility enable them to acheive large gape sizes and "walk" over their prey? We are using XROMM to measure the kinematics of the braincase, hemimandibles, quadrates, maxilla, palatines, and pterygoids during intraoral prey transport in reticulated pythons.

The origin of air breathing required the evolution of a new structure (lungs) and a new behavior (surfacing, expiring air, and inspiring air), which posed the biomechanical challenge of transporting air into and out of the lungs. Fish solved this problem by using 'buccal pumping,' which is also the biomechanical basis of suction feeding and gill ventilation, behaviors that had evolved long before air breathing. Are the morphology and mechanics of suction feeding (aquatic buccal pumping) well suited for air breathing (aerial buccal pumping)? I used XROMM to quantify skeletal kinematics during these two behaviors in West African lungfish and found that the origin of air breathing likely did not require substantial changes to cranial kinematics or morphology, despite interacting with a different physical medium, air.

Extant lungfishes have fewer mobile cranial bones than most actinopterygian fishes—they don't have a mobile maxilla, premaxilla, or suspensoria, and their opercula are reduced to slivers. However, they do have paired cranial ribs, which are unique to lungfishes. The role of the cranial ribs, as well as the pectoral girdle (which is also located at the back of the head and difficult to measure), during buccal pumping behaviors was unknown. Do the cranial ribs, pectoral girdle, and their associated muscles play an active role during suction feeding and air breathing? We found that they do—in addition to serving as anchors for muscle shortening, the cranial ribs and pectoral girdle rotated consistently, contributing to buccal expansion.

When studying feeding form and function, the obvious region of interest is the head. But in suction feeding fishes, there is evidence that they use their whole bodies to generate suction power. Is postcranial morphology a strong predictor of feeding biomechanics? We explored this hypothesis in royal knifefish, and in comparison to bluegill sunfish, largemouth bass, and channel catfish (species whose suction power had previously been measured with XROMM). We found that features of the postcranial morphology of royal knifefish enabled them to recruit vertebral column bending to enhance buccal expansion and generate power. This research provides support that feeding behaviors have likely shaped the evolution of the axial muscles and skeleton.

All skeletal muscles produce their largest forces at a single optimal length, losing force when stretched or shortened. In vertebrate feeding systems, this fundamental force–length relationship translates to variation in bite force across gape, which affects the food types that can be eaten effectively. We measured the bite force–gape curves of two sympatric species: king salmon and pink salmon. Cranial anatomical measurements were not significantly different between species; however, peak bite forces were produced at significantly different gapes. This may allow king salmon to use greater force when eating large or elusive prey. In contrast, pink salmon do not require high forces at extreme gapes for filter feeding. Our results illustrate that the bite force–gape relationship is an important ecophysiological axis of variation.