How does evolution shape bones and muscles that are used in multiple biomechanical systems ? This question has inspired my interest in fish gill ventilation. Gill ventilatory pumping in fishes requires the use of more than 20 individual bones and 8 distinct muscles, most of which are also used in feeding and other behaviors. This overlap in structures among functions is known as "functional coupling," which is thought to constrain morphological evolution. However, fish skulls are incredibly diverse. Is functional coupling really so constraining after all? If so, are there mechanisms for relaxed constraint in some lineages, allowing them to become morphologically diverse? These are the questions that I hope to answer in my research. Check out my Google Scholar profile and the descriptions below to read about my work.
The basics of fish gill ventilation
Ray-finned fishes (Actinopterygii) ventilate their gill tissue by pumping water into the mouth, over the gills, and out the gill openings. This allows water to flow in a single direction over the microstructures of the gills, setting up a countercurrent gas exchange system with the bloodstream, which flows through the respiratory tissue in the opposite direction.
However, getting water to flow in one direction is not so easy. To do this, fishes take advantage of the fact that fluids move from areas of high pressure to low pressure. They use cyclical pumping of the mouth and gill chambers (Figs. 1 and 2), which are expanded and compressed by many bones and muscles. Expansion of a chamber generates negative pressure, and compression of a chamber generates positive pressure. Check out the animation (Fig. 2) to see the pattern of flow through a fish skull.
The fish that breathes out its armpit.
We can learn a lot about the evolution of a biomechanical system by studying extreme cases— animals that "break the rules." For gill ventilation, the Goosefish (Lophius americanus) is a great example of this, because they breathe incredibly slowly. Goosefish are bottom-dwellers that blend in with the sandy ocean floor and ambush prey. They are anglerfishes, and therefore they have a lure for attracting prey (Fig. 3). You may have eaten a goosefish - they are called "monkfish" in the culinary world!
An average goosefish takes over a minute to complete one ventilatory cycle (Farina and Bemis, 2016), and bigger goosefish take even longer (up to 5 minutes)! This is more than 100 times slower than a goldfish! This makes it much easier for them to hide their ventilatory movements from predators and prey. Their slow breathing is possible only because of their gigantic gill chambers, which extend underneath the pectoral fins and end with the gill opening positioned in the "armpit" of the fish (Fig. 3). They have specialized musculature, which we describe in our paper, to hold the gill opening in a siphon-like shape during exhale. Watch the video below to see this in action!
Farina, SC, WE Bemis. 2016. Functional morphology of gill ventilation in the Goosefish, Lophius americanus (Lophiiformes: Lophiidae). Zoology. 119:207-215.
Evolution of gill ventilation
So how does the goosefish help us to understand such a complex system shared by all 30,000+ species of ray-finned fishes? Their gill chambers are highly specialized in two ways: they have extremely elongate branchiostegal rays and a small gill opening. I have investigated the function and evolutionary history of both of these adaptations across ray-finned fishes.
I completed a large-scale phylogenetic survey of gill opening morphology across 433 families of ray-finned fishes. My co-authors and I found that tiny, restricted gill openings have evolved independently more than 20 times in at least 11 major clades. 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 concluded that this specialized gill opening morphology likely evolved for very different functions in different lineages, including providing greater stability of the branchiostegal apparatus, allowing opercular jetting for burial and locomotion, and providing evolutionary flexibility in gill opening position.
Farina, SC, TJ Near, WE Bemis. 2015. Evolution of the branchiostegal membrane and restricted gill openings in actinopterygian fishes. Journal of Morphology 276:681-694.
To further explore the evolution and function of the gill ventilatory system, I focused on the Cottoidei (sculpins and relatives), a group of bottom-dwelling fishes with considerable variation in cranial morphology. I measured ventilatory pressures in the mouth and gill chambers of four sculpins and found that pressures differed greatly among species. Much of the pressure variation was explained by the size of the branchiostegals. Branchiostegal rays (see Fig. 1) support the gill chamber and contribute substantially to ventilatory pumping.
Farina, SC, LA Ferry, M Knope, AP Summers, and WE Bemis. The contribution of the branchiostegal apparatus to driving ventilatory current in cottoid fishes. Society for Integrative and Comparative Biology. West Palm Beach, FL. January
I then used micro-CT reconstructions to analyze cranial bones in 20 cottoids. I found that the jaws, opercular bones, and branchiostegals are evolutionarily integrated with one another, while the hyoid (the bony tongue) did not show integration with any other cranial unit, despite being a critical structure in both suction feeding and gill ventilation. This suggests that the hyoid is an evolutionary module of the skull of cottoids. The overlap in morphology between suction feeding and gill ventilation in ray-finned fishes has the potential to severely limit morphological evolution, but modularity likely reduces these limitations.
Farina, SC, M Knope, KA Corn, AP Summers, and WE Bemis. Modularity and coupling in the evolution of the feeding and respiratory systems of cottoid fishes. Society for Integrative and Comparative Biology. Portland, OR. January 2016.
Hydrodynamic tradeoffs in microstructures of fish gills
The microstructures of gills act as biological microfluidic devices by passively altering the flow of water through the gills. I study the hydrodynamic and physiological consequences of variation in gill microstructure morphology. Gills consist of primary lamellae that extend from the gill arches and bear microscopic plates of tissue called secondary lamellae, which provide surface area for gas and ion exchange. I used scanning electron microscopy to survey gill morphology to create computational fluid dynamics models of lamellae (Fig. 4). By modeling flow rate, I have identified a hydrodynamic trade-off between efficiency and effectiveness of individual lamellae. While pelagic species are optimized for lamellae efficiency, the lamellae of benthic species are more effective individually.
Farina, SC. Virtual fish gills: Computational modeling to examine hydrodynamic trade-offs in gill microstructures. Society for Integrative and Comparative Biology. New Orleans, LA. January 2017.
Novel forms of locomotion in marine habitats
In addition to gill ventilation, I also study marine vertebrates that have evolved novel behaviors in place of swimming. When an aquatic animal must escape stress due to the presence of a predator or poor water conditions, swimming away is not always a viable option. I have collaborated with undergraduates at Cornell University (CU), Shoals Marine Laboratory (SML), and Friday Harbor Laboratories (FHL) to study animals that have evolved alternatives to swimming. I worked with William Gough (CU ’14) and Dr. Frank Fish at West Chester University to study eider ducks hydroplaning along the water to escape predation. I also worked with Noah Bressman (CU ’16) and Dr. Alice Gibb at Northern Arizona University to study how mummichogs (small intertidal fishes at SML) navigate on land as they jump between pools6. At FHL, I am a part of a working group led by Dr. Adam Summers on fluid dynamics and scaling effects of burial behaviors, and I have worked with a graduate student (Amberle McKee, UC Irvine) and an undergraduate (Katherine Corn, CU ’16) as they studied flatfish burial.
Publications and presentations on the above studies:
Gough, WT, SC Farina, FE Fish. 2015. Aquatic burst locomotion by hydroplaning and paddling in common eiders (Somateria mollissima). Journal of Experimental Biology 218:1632-1638.
McKee, A, I MacDonald, SC Farina, AP Summers. 2015. Undulation frequency affects burial performance in living and model flatfishes. Zoology 119:75-80
Bressman, NR, SC Farina, AC Gibb. 2016. Look before you leap: visual navigation and terrestrial locomotion of the intertidal killifish Fundulus heteroclitus. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 325:57-64.
Corn, KA, SC Farina, AC Gibb, and AP Summers. Scaling of burial mechanics in Parophrys vetulus, the English Sole. Society for Integrative and Comparative Biology. Portland, OR. January 2016.
Bressman, NR, SC Farina, and AC Gibb. A comparative analysis of the novel terrestrial locomotion of the tidepool sculpin, Oligocottus maculosus. Society for Integrative and Comparative Biology. Portland, OR. January 2016.
Collaborations on fish feeding
I have also worked with undergraduate mentees Katherine Corn and Alexus Roberts (both now PhD students in the Wainwright Lab at UC Davis) on studies of fish feeding, including cutting performance of shark teeth and evolution of jaw mechanics in sculpins.
Corn, KA, SC Farina, J Brash, AP Summers. 2016. Modelling tooth-prey interactions in sharks - the importance of dynamic testing. Royal Society Open Science 3:160141. http://rsos.royalsocietypublishing.org/content/3/8/160141
Roberts, AS, SC Farina, and NJ Gidmark. Feeding mechanics and functional morphology in jaws of sculpins. Society for Integrative and Comparative Biology. Portland, OR. January 2016.
Figure 1. These are the bones that make up the mouth and gill chambers of ray-finned fishes. The jaws and hyoid (bony tongue) expand and compress the mouth chamber, and the operculars and branchiostegals actuate the gill chamber. The gill arches (white in bottom figure) hold the gill tissue and sit between the two chambers.
Figure 2. Here is a model of fish ventilation fluid dynamics, in which the complex 3D structure of the fish skull has been reduced to pistons in a pump. Fishes alternate between generating negative pressure and positive pressure to draw water over the gills.
Figure 3. The Goosefish (Lophius americanus) has an enormous gill chamber that ends in a small gill opening behind the pectoral fin. This chamber fills incredibly slowly, allowing the goosefish to remain hidden from prey and predators.
Figure 4. Modeling the microstructures of fish gills. I use models of fluid dynamics (top) to quantify the effects of variation in secondary lamellae (bottom; SEM image) on gill water flow.
Contact
Email: scf59 at cornell dot edu
Twitter: @stacyfarina