Blowfly uses saliva to keep cool

Insect moves droplet of saliva in and out of mouth to promote evaporation and lower body temperature, according to study by researchers in Brazil.

By Elton Alisson  |  Agência FAPESP – On warm days the Oriental latrine blowfly (Chrysomya megacephala) keeps cool by moving a droplet of saliva repeatedly in and out of its buccal apparatus, or mouth, and then swallowing it.

Researchers at the University of São Paulo’s São Carlos Physics Institute (IFSC-USP) in Brazil, in collaboration with colleagues at São Paulo State University’s Bioscience Institute in Rio Claro (IBRC-UNESP), have found that the saliva droplet cools through evaporation during this “tidal” movement. Ingestion of the droplet then cools important parts of the insect’s body such as its flight muscles and brain.

The discovery was made during Guilherme Gomes’s postdoctoral research at IFSC-USP, with a scholarship from FAPESP, and as part of a project conducted by researchers at IBRC-UNESP, also with FAPESP’s support, and has just been described in a paper published in Scientific Reports.

“We observed that this behavior, known as ‘bubbling’, enables blowflies to lower their body temperature considerably,” Gomes told Agência FAPESP.

The researchers used a thermographic camera to record the activities of adult blowflies during a period of several days. The insects were kept in a thermally insulated climate chamber equipped to detect temperature-related infrared radiation.

“The thermographic camera enabled us to monitor surface temperature changes occurring in a matter of seconds,” said Denis Otávio Vieira de Andrade, a professor at IBRC-UNESP and one of the authors of the study.

The recordings showed that these blowflies engineered evaporative cooling by tidally moving a droplet of fluid out of their buccopharyngeal cavity and back inside it again, in sequential cycles of between one and 15 times in a few seconds. Analysis of the infrared images revealed that repetition of the cycle cooled the droplet as much as 8 °C below ambient temperature within 15 seconds.

The droplet was then swallowed, lowering the temperature of the head, thorax and abdomen by 1 °C, 0.5 °C, and 0.2 °C respectively. As the cycle was repeated, the temperature of the same body parts decreased 3 °C, 1.6 °C, and 0.8 °C respectively.

“When the fly moves this cooled droplet into its buccal apparatus, it lowers the temperature first of its head, then of its thorax, and finally of its abdomen,” Gomes said.

Frequency variation

The researchers also observed variations in the frequency of bubbling behavior to bring about evaporative cooling in accordance with ambient temperature and humidity, and with the insects’ activity and heat production.

At temperatures below 25 °C, when they are highly active and need to warm up their flight muscles in order to be able to fly efficiently, bubbling would cause an unwanted drop in temperature and in fact this behavior was not observed.

Bubbling began in the range of 25-30 °C to deploy heat dissipation via evaporative cooling and hence regulate body temperature. However, when relative humidity exceeded 70% the droplet cooling mechanism was not observed as it would not work without evaporation transition.

The blowflies also used bubbling to keep cool at night, especially when it was very warm. “They lowered body temperature between 2 °C and 3 °C for eight hours during the night by repeating this behavior every 30 or 60 minutes,” Gomes said.

The heightened frequency of bubbling at night probably benefits the insects because lower body temperature reduces metabolic expenditure and saves energy during a period of inactivity.

Some humming-birds use a similar strategy, falling into a sleep-like state known as torpor to conserve energy at night when they cannot forage. This involves a drastically lowered metabolic rate and body temperature.

“If the flies’ body temperature remained high at night they would have a high metabolic rate and use up most of their energy reserves,” Gomes said. “By cooling mainly the head, they can reduce the cost of processing vision and high-energy tissue in the brain.”

Thermographic video shot during blowfly's bubbling behavior (video: Guilherme Gomes / IFSC-USP)

Efficient flight

The droplet exuded by the blowfly to lower its body temperature comprises a complex mixture of enzymes from salivary glands, antimicrobials associated with the digestive system, and substances from ingested meals.

A foraging blowfly dilutes food with salivary secretions and then sucks up the mixture formed by the food substrate, its own saliva, and enzymes from its salivary glands. In landing elsewhere and repeating this behavior, it disperses droplets of the mixture and may transmit disease.

“The evolution of these blowflies developed the bubbling mechanism to associate two key functions: cutting energy expenditure during flight by reducing inert matter weight, and thermoregulation, which keeps body temperature in the ideal range. This mechanism partly uses the same physical principles as sweating in humans and panting in dogs,” Gomes said.

Using the data obtained from the experiments, the researchers built a mathematical model to understand and describe the saliva droplet evaporation process and calculate the optimal droplet diameter to obtain rapid evaporation.

“We applied basic energy conservation principles to this case in order to model the dynamics of heat transfer during the insect’s behavior,” said physicist Roland Köberle, a professor at IFSC-USP and a co-author of the study.

The article “Droplet bubbling evaporatively cools a blowfly” (doi: 10.1038/s41598-018-23670-2) by Guilherme Gomes, Roland Köberle, Claudio J. Von Zuben and Denis V. Andrade can be read in the journal Scientific Reports at nature.com/articles/doi:10.1038/s41598-018-23670-2.