Development and application of a novel biologging tag to estimate the metabolic rates of free-swimming sharks

Abstract

An organism’s metabolism underpins and determines the rate of every other biological process and activity. It also influences how an animal both acquires and uses resources as well as how it interacts with its environment. Despite this fact, a relatively limited number of species of elasmobranch (sharks, skates, and rays) have had any research done into determining these rates. This is due to limitations on both the acquisition and transport of animals from the field as well as size constraints of equipment available for measuring metabolic rates in aquatic organisms. Metabolic rates that have been measured in a laboratory setting are generally not representative of metabolic rates exhibited by animals in the wild, when animals are moving through a dynamic environment and exhibiting different behaviors. In this dissertation, I develop, validate, and test a novel biologging tag which we hope will help address these difficulties in measuring accurate metabolic rates for larger and free swimming, water breathing animals. ☐ The RemO2ra tag operates by measuring both the dissolved oxygen content of ambient seawater and exhalant from the gill via two fiber-optic oxygen sensors. ☐ I first deployed a version of the tag on a captive Lemon Shark (Negaprion brevirostris) at a Ripley’s Aquarium holding facility in Buffalo NY to determine if the oxygen content of the gill exhalant (the water exiting the gills) would be representative of the level of extraction at the gills. I found a clear difference in the ambient percent oxygen saturation in the tank, reflecting the oxygen content of seawater passing over the gills, and the percent oxygen saturation of water leaving the gills. During this test, the shark participated in two distinct behaviors - sitting and swimming - and it was possible to observe differences in oxygen saturation at the gills between the two activities. There was a significant periodicity to the animal’s buccal pumping that had a strong positive correlation to video observations of the drawing in and expelling of water that was occurring at the gills. ☐ Once it was established that we could observe a clear sign of oxygen consumption at the gills via the sensor probe, laboratory-based experiments were used to develop a methodology for calculating a whole animal metabolic rate (ṀO2) from a single sensor at the center of the third gill. This was accomplished via flow through respirometry with sedated Sandbar Sharks (Carcharhinus plumbeus). Concurrent tank and gill-based oxygen consumption measurements were taken over a period of 30 minutes, with a 15-minute background reading taken after the animal was removed from the tank. A sensitivity analysis was used to determine the rate of flow reduction that occurs as the water moves through the oropharyngeal cavity due to friction, meaning the difference between flow rate as water entered the animals’ mouth, and when it left the gills, which found an average true ventilation volume of 62% of the maximum ventilation volume. A one sample t-test was used to compare the tank-based ṀO2 rates and the gill-based ṀO2 rates using the corrected ventilation volume for each shark and found no significant difference between the two (p = 0.981). ☐ The ultimate objective of developing this methodology and tag is to deploy the tag on free-swimming animals. Now that I had developed a method for obtaining a reliable, full animal ṀO2 rate via oxygen exhalant data taken from the center of the third gill, we used the same process to compare rates on free swimming animals. During the summer of 2024, four juvenile Sandbar Sharks were collected from Delaware Bay and used for respirometry trials in a dock-based floating respirometer. During trials, a shark was fitted with the tag and placed in the respirometer to swim freely. As with the previous set of experiments, concurrent tank- and gill-based measurements were taken. For this iteration of the tag, we did not yet have an integrated flow sensor. Sensitivity testing was used to determine both a true ventilation volume and average flow speed in the system. Again, there was no significant difference found between the gill-based ṀO2 rate and the tank-based rates (p = 0.4039). In March of 2025, similar trials were conducted with juvenile Bull Sharks (Carcharhinus leucas) in Vero Beach, FL. This iteration of the tag was fitted with a flow sensor, which allowed us to use flow speed as a representation of the animal’s swimming speed, which we used to estimate flow of water over the gills during ram ventilation. There was also no significant difference found between the respirometer and tag rates (p = 0.7234). When analyzing the data for the Bull Shark trials, I also calculated an instantaneous gill-based ṀO2 rates, taking into consideration that we would not have a measurable slope for the free-swimming sharks. There was no significant difference between this rate and the tank-based rate (p = 0.8497) or the respR calculated gill-based rate (p = 0.8717). This method allows for a data-point by data-point estimate of ṀO2. ☐ Finally, having established the tag’s functionality, and the ability to calculate an ṀO2 with the data, I deployed the tag in the wild on a free-swimming Bull Shark in Florida during March of 2025. The animal carried the tag for 18 hours and 57 minutes. During that time, it swam from the Indian River Lagoon into Sebastian Creek, a major freshwater tributary of the Lagoon. From the ambient and gill-based oxygen, flow and gape data, using the instantaneous method, I was able to estimate an ṀO2 rate for each data point. The metabolic rates are comparable to those found in the literature, but also varied across time and environmental circumstances. More work needs to be done to refine our understanding of ventilatory flow and the reduction that occurs compared to swimming speed, but this does show that we are able to calculate a ṀO2 rate for a free-swimming shark with this tag, as well as to observe changes in said rate as the animal moves through its environment.