In a study published Oct. 28 in the Journal of Experimental Biology, an international team of researchers studying the unique fluid environments of blue whales traveling off the coast of Palos Verdes and San Diego, CA has reported capturing the first-ever continuous recording of remora behavior on a host organism, using advanced biosensing tags with video recording capabilities.

The study shows the secrets behind the remora fish’s success in hitchhiking aboard baleen whales more than 30 times their size to safely traverse the ocean — they select the most flow-optimal regions on the whale’s body to stick to, such as behind the whale’s blowhole, where drag resistance for the fish is reduced by as much as 84%. The team’s findings also show that remoras can freely move around to feed and socialize on their ride even as their whale host hits burst speeds of more than 5 meters per second, by utilizing previously unknown surfing and skimming behaviors along special low-drag traveling lanes that exist just off the surface of the whale’s body.

Researchers say the study represents the highest-resolution whole-body fluid dynamic analysis of whales to date, the insights from which could potentially be used as a basis to better understand the behavior, energy use and overall ecological health of the species, as well as improve tagging and tracking of whales and other migratory animals in future studies.

“Whales are like their own floating island, basically like their own little ecosystems. …To get a look into the flow environment of blue whales within a millimeter resolution through this study is extremely exciting,” said Brooke Flammang, assistant professor of biology at New Jersey Institute of Technology and the study’s corresponding author. “Through lucky coincidence, our recordings captured how remoras interact in this environment and are able to use the distinct flow dynamics of these whales to their advantage. It is incredible because we’ve really known next to nothing about how remoras behave on their hosts in the wild over any prolonged period of time.”

Until now, scientists studying the symbiotic relationships between remoras and their hosts in their natural ocean habitat have predominantly relied on still images and anecdotal evidence, leaving much of how they go about their renown sticking behavior beneath the surface a mystery.

In their recent investigation, the researchers employed multi-sensor biologging tags with dual cameras that they attached to the whales via four 2-inch suction disks. The tags were able to calculate various measurements inside the whale’s ecosystem, such as surface pressure and complex fluid forces around the whales, as well as GPS location and traveling speeds through tag vibrations, all while video recording the remoras at 24 frames per second and 720p resolution.

“Fortunately, the drag on dimple-shaped airplane cockpits has been measured many times and we were able to apply this knowledge to help figure out the drag these remoras were experiencing,” said Erik Anderson, co-author, biofluid dynamics researcher at Grove City College and guest investigator at the Woods Hole Oceanographic Institution. “But our study still required calculating, for the first time ever, the flow over a blue whale using computational fluid dynamics … it took an international team of biologists, programmers, engineers and a supercomputer to do that.”

The team’s 211 minutes of video footage and whale tag data processed by researchers at the Barcelona Supercomputing Center captured a total of 27 remoras at 61 locations on the whales overall, finding that the remoras were most often podding and traveling between three of the most hydrodynamically beneficial spots where separating flow and wakes are caused by the whale’s distinct topographical features: directly behind the blowhole, next to and behind the dorsal fin, and the flank region above and behind the pectoral fin.

According to the team’s measurements, Anderson says that the shear force experienced by an average-sized remora in the wake behind the blow hole of a whale swimming at the casual speed of 1.5 m/s can be as low as 0.02 Newtons, half the force of drag in the free stream above. However, Anderson notes that the average remora’s suction force of 11-17 Newtons is more than a match for even the most intense parking spot on the whale, its tail, where the remora experiences roughly 0.14 Newtons of shear force. And though the forces are greater, the same is true even for large remora riding on whales swimming at much higher speeds.

“We learned that the remora’s suction disk is so strong that they could stick anywhere, even the tail fluke where the drag was measured strongest, but they like to go for the easy ride,” said Erik Anderson. “This saves them energy and makes life less costly as they hitchhike on and skim over the whale surface like a NASA probe over an asteroid or some mini-world.”

Remoras Go Surf’s Up

The tags showed that to conserve energy while getting about on their floating island, the remoras take advantage of the whale’s physics by surfing inside a thin layer of fluid surrounding the whale’s body, known as a boundary layer, where the team found drag force is reduced by up to 72% compared to the much more forceful free stream just above. Flammang says the fishes can lift within 1cm from their host in this layer to feed or join their mates at other low-drag social spots on the whale, occasionally changing directions by skimming, or repeatedly attaching and releasing their suction disks on the whale’s body.

Flammang suspects that remoras are able to move freely without being completely peeled from their speedy hosts, which can move nearly seven times faster than the remora, through something called the Venturi effect.

“The skimming and surfing behavior is amazing for many reasons, especially because we think that by staying about a centimeter off the whale body, they are taking advantage of the Venturi effect and using suction forces to maintain their close proximity,” explained Flammang. “In this narrow space between the remora and whale, when fluid is funneled into a narrow space it moves at a higher velocity but has lower pressure, so it is not going to push the remora away but can actually suck it toward the host. They can swim up into the free stream to grab a bite of food and come back down into the boundary layer, but it takes a lot more energy to swim in the free stream flow.”

Along with uncovering new details of the remora’s hitchhiking prowess, the team says they will continue to explore both the flow environments around whales and the mechanisms by which specifically adapted organisms like remoras successfully attach to hosts in order to improve animal tag technologies and designs for extended periods of behavioral and ecological monitoring. The team is also using their new insights into the remora’s preferred low-drag attachment locations to better inform where they might tag whales in studies to come.

“It’s an extremely arduous process to study whales what with permitting, research regulations and the game of chance of finding animals, all for the tags to usually fall off within 48 hours,” said Flammang. “If we can come up with a better way to collect longer term data through better tag placement or better technologies, it could really advance our learning of the species, and many other animals that remoras attach to.”

This circuit is particularly important for learning to make decisions that require evaluating the cost and reward that come with a particular action. The researchers showed that they could boost older mice’s motivation to engage in this type of learning by reactivating this circuit, and they could also decrease motivation by suppressing the circuit.

“As we age, it’s harder to have a get-up-and-go attitude toward things,” says Ann Graybiel, an Institute Professor at MIT and member of the McGovern Institute for Brain Research. “This get-up-and-go, or engagement, is important for our social well-being and for learning — it’s tough to learn if you aren’t attending and engaged.”

Graybiel is the senior author of the study, which appears today in Cell. The paper’s lead authors are Alexander Friedman, a former MIT research scientist who is now an assistant professor at the University of Texas at El Paso, and Emily Hueske, an MIT research scientist.

Evaluating cost and benefit

The striatum is part of the basal ganglia — a collection of brain centers linked to habit formation, control of voluntary movement, emotion, and addiction. For several decades, Graybiel’s lab has been studying clusters of cells called striosomes, which are distributed throughout the striatum. Graybiel discovered striosomes many years ago, but their function had remained mysterious, in part because they are so small and deep within the brain that it is difficult to image them with functional magnetic resonance imaging (fMRI).

In recent years, Friedman, Graybiel, and colleagues including MIT research fellow Ken-ichi Amemori have discovered that striosomes play an important role in a type of decision-making known as approach-avoidance conflict. These decisions involve choosing whether to take the good with the bad — or to avoid both — when given options that have both positive and negative elements. An example of this kind of decision is having to choose whether to take a job that pays more but forces a move away from family and friends. Such decisions often provoke great anxiety.

In a related study, Graybiel’s lab found that striosomes connect to cells of the substantia nigra, one of the brain’s major dopamine-producing centers. These studies led the researchers to hypothesize that striosomes may be acting as a gatekeeper that absorbs sensory and emotional information coming from the cortex and integrates it to produce a decision on how to act. These actions can then be invigorated by the dopamine-producing cells.

The researchers later discovered that chronic stress has a major impact on this circuit and on this kind of emotional decision-making. In a 2017 study performed in rats and mice, they showed that stressed animals were far more likely to choose high-risk, high-payoff options, but that they could block this effect by manipulating the circuit.

In the new Cell study, the researchers set out to investigate what happens in striosomes as mice learn how to make these kinds of decisions. To do that, they measured and analyzed the activity of striosomes as mice learned to choose between positive and negative outcomes.

During the experiments, the mice heard two different tones, one of which was accompanied by a reward (sugar water), and another that was paired with a mildly aversive stimulus (bright light). The mice gradually learned that if they licked a spout more when they heard the first tone, they would get more of the sugar water, and if they licked less during the second, the light would not be as bright.

Learning to perform this kind of task requires assigning value to each cost and each reward. The researchers found that as the mice learned the task, striosomes showed higher activity than other parts of the striatum, and that this activity correlated with the mice’s behavioral responses to both of the tones. This suggests that striosomes could be critical for assigning subjective value to a particular outcome.

“In order to survive, in order to do whatever you are doing, you constantly need to be able to learn. You need to learn what is good for you, and what is bad for you,” Friedman says.

“A person, or this case a mouse, may value a reward so highly that the risk of experiencing a possible cost is overwhelmed, while another may wish to avoid the cost to the exclusion of all rewards. And these may result in reward-driven learning in some and cost-driven learning in others,” Hueske says.

The researchers found that inhibitory neurons that relay signals from the prefrontal cortex help striosomes to enhance their signal-to-noise ratio, which helps to generate the strong signals that are seen when the mice evaluate a high-cost or high-reward option.

Loss of motivation

Next, the researchers found that in older mice (between 13 and 21 months, roughly equivalent to people in their 60s and older), the mice’s engagement in learning this type of cost-benefit analysis went down. At the same time, their striosomal activity declined compared to that of younger mice. The researchers found a similar loss of motivation in a mouse model of Huntington’s disease, a neurodegenerative disorder that affects the striatum and its striosomes.

When the researchers used genetically targeted drugs to boost activity in the striosomes, they found that the mice became more engaged in performance of the task. Conversely, suppressing striosomal activity led to disengagement.

In addition to normal age-related decline, many mental health disorders can skew the ability to evaluate the costs and rewards of an action, from anxiety and depression to conditions such as PTSD. For example, a depressed person may undervalue potentially rewarding experiences, while someone suffering from addiction may overvalue drugs but undervalue things like their job or their family.

The researchers are now working on possible drug treatments that could stimulate this circuit, and they suggest that training patients to enhance activity in this circuit through biofeedback could offer another potential way to improve their cost-benefit evaluations.

“If you could pinpoint a mechanism which is underlying the subjective evaluation of reward and cost, and use a modern technique that could manipulate it, either psychiatrically or with biofeedback, patients may be able to activate their circuits correctly,” Friedman says.

The research was funded by the CHDI Foundation, the Saks Kavanaugh Foundation, the National Institutes of Health, the Nancy Lurie Marks Family Foundation, the Bachmann-Strauss Dystonia and Parkinson’s Foundation, the William N. and Bernice E. Bumpus Foundation, the Simons Center for the Social Brain, the Kristin R. Pressman and Jessica J. Pourian ’13 Fund, Michael Stiefel, and Robert Buxton.

Over time, however, and in more recent years, lower body temperatures have been widely reported in healthy adults. A 2017 study among 35,000 adults in the United Kingdom found average body temperature to be lower (97.9°F), and a 2019 study showed that the normal body temperature in Americans (those in Palo Alto, California, anyway) is about 97.5°F.

A multinational team of physicians, anthropologists and local researchers led by Michael Gurven, UC Santa Barbara professor of anthropology and chair of the campus’s Integrative Anthropological Sciences Unit, and Thomas Kraft, a postdoctoral researcher in the same department, have found a similar decrease among the Tsimane, an indigenous population of forager-horticulturists in the Bolivian Amazon. In the 16 years since Gurven, co-director of the Tsimane Health and Life History Project, and fellow researchers have been studying the population, they have observed a rapid decline in average body temperature — 0.09°F per year, such that today Tsimane body temperatures are roughly 97.7°F.

“In less than two decades we’re seeing about the same level of decline as that observed in the U.S. over approximately two centuries,” said Gurven. Their analysis is based on a large sample of 18,000 observations of almost 5,500 adults, and adjust for multiple other factors that might affect body temperature, such as ambient temperature and body mass.

The anthropologists’ research appears in the journal Sciences Advances.

“The provocative study showing declines in normal body temperature in the U.S. since the time of the Civil War was conducted in a single population and couldn’t explain why the decline happened,” said Gurven. “But it was clear that something about human physiology could have changed. One leading hypothesis is that we’ve experienced fewer infections over time due to improved hygiene, clean water, vaccinations and medical treatment. In our study, we were able to test that idea directly. We have information on clinical diagnoses and biomarkers of infection and inflammation at the time each patient was seen.

While some infections were associated with higher body temperature, adjusting for these did not account for the steep decline in body temperature over time, Gurven noted. “And we used the same type of thermometer for most of the study, so it’s not due to changes in instrumentation,” he said.

Added Kraft, “No matter how we did the analysis, the decline was still there. Even when we restricted analysis to the <10% of adults who were diagnosed by physicians as completely healthy, we still observed the same decline in body temperature over time.”

A key question, then, is why body temperatures have declined over time both for Americans and Tsimane. Extensive data available from the team’s long-term research in Bolivia addresses some possibilities. “Declines might be due to the rise of modern health care and lower rates of lingering mild infections now as compared to the past,” Gurven explained. “But while health has generally improved over the past two decades, infections are still widespread in rural Bolivia. Our results suggest that reduced infection alone can’t explain the observed body temperature declines.”

It could be that people are in better condition, so their bodies might be working less to fight infection, he continued. Or greater access to antibiotics and other treatments means the duration of infection is shorter now than in the past. Consistent with that argument, Gurven said, “We found that having a respiratory infection in the early period of the study led to having a higher body temperature than having the same respiratory infection more recently.”

It’s also possible that greater use of anti-inflammatory drugs like ibuprofen may reduce inflammation, though the researchers found that the temporal decline in body temperature remained even after their analyses accounted for biomarkers of inflammation.

“Another possibility is that our bodies don’t have to work as hard to regulate internal temperature because of air conditioning in the summer and heating in the winter,” Kraft said. “While Tsimane body temperatures do change with time of year and weather patterns, the Tsimane still do not use any advanced technology for helping to regulate their body temperature. They do, however, have more access to clothes and blankets.”

The researchers were initially surprised to find no single “magic bullet” that could explain the decline in body temperature. “It’s likely a combination of factors — all pointing to improved conditions,” Gurven said.

According to Gurven, the finding of lower-than-expected body temperatures in the U.S., and the decline over time, had a lot of people scratching their heads. Was it a fluke? In this study, Gurven and his team confirm that body temperatures below 98.6°F are found in places outside the U.S. and the U.K. “The area of Bolivia where the Tsimane live is rural and tropical with minimal public health infrastructure,” he noted. “Our study also gives the first indication that body temperatures have declined even in this tropical environment, where infections still account for much morbidity and mortality.”

As a vital sign, temperature is an indicator of what’s occurring physiologically in the body, much like a metabolic thermostat. “One thing we’ve known for a while is that there is no universal ‘normal’ body temperature for everyone at all times, so I doubt our findings will affect how clinicians use body temperature readings in practice” said Gurven. Despite the fixation on 98.6°F, most clinicians recognize that ‘normal’ temperatures have a range. Throughout the day, body temperature can vary by as much as 1°F, from its lowest in the early morning, to its highest in the late afternoon. It also varies across the menstrual cycle and following physical activity and tends to decrease as we age.

But by linking improvements in the broader epidemiological and socioeconomic landscape to changes in body temperature, the study suggests that information on body temperature might provide clues to a population’s overall health, as do other common indicators such as life expectancy. “Body temperature is simple to measure, and so could easily be added to routine large-scale surveys that monitor population health,” Gurven said.