Biomechanics in a changing world

Biomechanics in a changing world 

Mussel mesocosms. Photo: Emily Carrington

Climate change is a phenomenon widely studied by ecologists and animal physiologists, but there are also many important biomechanical pieces that need to be added in order to complete the puzzle. Frank Seebacher and Paolo Domenici, organisers of the ‘Climate Change and Biomechanics’ session, were excited to bring together researchers from a range of disciplines for an exciting and increasingly important discussion. “We are both interested in the effects of climate change on organisms and felt that the field of biomechanics had a lot to offer,” explains Paolo. As global temperatures rise and the oceans become more acidic, it is important to understand both the small and large-scale effects of environmental change on all aspects of animal life – and experimental biomechanical research allows researchers to predict what real-world climate shifts are likely to mean for our planet’s wildlife. “We were pleased with the range of topics covered during the session and we hope that they will help to inspire more integrated research into biomechanics and climate change,” Paolo adds.

JUST KEEP SWIMMING

Paolo’s own research interests are currently invested in understanding the effects of climate change on fish swimming performance and behaviour. Marine life serves as a useful range of organisms to study in the context of climate change due to the large number of environmental changes caused by climate shifts such as increased sea temperatures, ocean acidification and hypoxia. “Marine organisms are facing many simultaneous stressors and it is fundamental to understand their impact on how these animals function and the potential for ecological repercussions,” explains Paolo. For many marine species, the ability to swim is crucial for their survival, especially when it comes to hunting or avoiding their own hunters. According to Paolo “Burst swimming performance will largely determine if prey will be successful at escaping predation, but there are also other important behavioural factors besides performance, such as responsiveness and escape direction”. These factors are essential in determining how fish will cope with the challenges of life, so how might they fare in the face of a changing climate?

Through a series of laboratory experiments he has conducted with Christel LeFrançois, a postdoctoral researcher now working at the University of La Rochelle in France, Paolo subjected various fish species to artificial threatening stimuli and analysed video footage of the resulting swimming responses¹. By exposing the fish to a range of environmental conditions prior to the challenging stimuli, they were able to investigate the effects of acclimation to low oxygen environments and demonstrate the effects of climate change induced hypoxia on anti-predator responses.

Paolo’s results showed that exposure to hypoxic conditions affected many aspects of fish swimming behaviour and performance, including directionality and responsiveness. “Although some sensory impairment was expected in hypoxic conditions, it was surprising to find that escape locomotion, which is fuelled anaerobically, is also affected by hypoxia,” says Paolo, adding that this may be due to the disruptive effects of hypoxia on the neurological mechanisms controlling escape responses. Building on this research, Paolo has also been working in collaboration with a team of researchers from James Cook University to investigate the relationship between escape performance in fish and ocean acidification, which is rapidly becoming another major concern for marine wildlife conservation. So, what do these biomechanical disruptions mean for the future of fish? Paolo suggests that the environmental effects of climate change could have major ecological repercussions by interfering with the outcome of predator-prey interactions. “Certain taxa, including avian predators, will not be directly affected by marine stressors such as ocean acidification or hypoxia,” Paolo explains, “which may lead to an imbalance in these predatorprey relationships”. While Paolo’s research highlights the importance of understanding these fundamental interactions between climate change and locomotor performance, he reminds us that our ability to meet the challenges of environmental change not only requires effective communication between researchers, but also with policymakers and the general public.

DEFENCE AGAINST THE SHARK ARTS

Spiny lobster. Photo: Kaitlyn Lowder

While some animal species will instinctively run, fly or swim away at the first sign of trouble, others have adapted to take more dynamic approaches to self-defence. One such species is the ecologically and economically significant California spiny lobster (Panulirus interruptus) which employs a wide range of defensive techniques in order to stave off potential predators such as sharks, octopuses and moray eels. But how effective will these techniques be in the strikingly different predicted environments of the future? Kaitlyn Lowder, a PhD student at the Scripps Institution of Oceanography, UC San Diego, hopes to answer this question and was excited to present her work exploring the effects of ocean acidification on the anti-predator defences of spiny lobsters. Previous research in this field has focused largely on the physiological costs of ocean acidification, but Kaitlyn’s interests are currently geared towards understanding the more functional consequences of these low pH environments: “The field of biomechanics provides the tools to study some of these lingering important questions”.

To test how altered pH and temperature conditions affect the different defence mechanisms of spiny lobsters, Kaitlyn built special flow-through water tanks where temperature and pH could be controlled and then exposed her animals to the reduced pH conditions predicted to occur by the year 2100. She then examined three key defences in the spiny lobster arsenal, including the kinematics of their anti-predator ‘tail-flips’, their responses to chemical cues, and the material properties of their antennae. While Kaitlyn has captured some beautiful slow-motion videos of their ‘tail flips’ in action, she admits that her spiny superstars are not always so graceful: “My favourite clip is of a lobster that rockets straight up and emerges from the water like Shamu… then lands with a total backflop!”

Kaitlyn’s experiments so far have revealed that, while some defences may be impaired by ocean acidification, others may remain unaffected. “Neither the speed and distance of the tail flip escapes nor the flexural stiffness of the antennae differed between the lobsters in today’s environmental conditions and those in future conditions,” Kaitlyn says, adding that this may be somewhat due to the abundance of food available during the experiments or the short nature of the experiments compared to the lobster’s natural moult cycle. “However, when I presented lobsters with a cue of a prey species, those in the lower pH conditions did not respond the same way that lobsters in today’s conditions did!” Kaitlyn goes on to suggest that this may be due to an impaired ability to detect or interpret chemical cues from the presence of the prey.

Speaking with Kaitlyn after the conference, it is clear that there are many more directions in which she wants to take this research, such as exploring how future environmental conditions may affect the material properties of spiny lobster exoskeletons and how their ability to handle prey might change if their mandibles are similarly affected. Finally, she highlights the importance of her research in the context of the sustainable harvesting of natural resources: “I hope my research can help fishery managers and fishers better look towards what is coming down the pipeline so that healthy fisheries can be maintained far into the future.”

THE WEAKEST LINK

Many molluscs provide key ecosystem services to humans and other organisms, such as improving water clarity through filter feeding, creating habitats for smaller creatures and providing a food source for a wide range of species including humans. Mussels are one such mollusc species that holds significant ecological and economic importance², but many of the services they provide rely on healthy biomechanical functions. One such function is the strong and stable attachment to substrates, which is primarily achieved through the deployment of organic byssal threads. “Byssal threads are golden flexible tethers, like bungee cords, that secure the animal to surfaces,” Emily Carrington from the University of Washington, USA explains. “If a mussel does not have a secure attachment, it falls to the seafloor and dies, usually eaten by hungry crabs or sea stars.” These byssal threads represent a key element of mussel survival and rely on specific mechanical and chemical processes in order to work properly, but how will these processes fare in the face of climate change?

Conducting experiments in both the laboratory and at a local mussel farm, Emily and colleagues were able to subject the mussels to controlled environmental conditions as well as more natural situations. The laboratory experiments took place in custom-built mesocosms at a range of pH and temperature conditions and ended with the harvesting of byssal threads for strength analysis, while less-regulated but more naturally variable experiments took place at the mussel farm. The results of their work demonstrate that when subjected to low pH, hypoxia or high temperature conditions (all environmental factors likely to worsen with climate change), these byssal threads can become much weaker and more likely to break under stress. Perhaps most intriguing, these different environmental factors seem to affect separate parts of the byssal structure in different ways. “We learned that high temperature impacts one part of a thread while low pH impacts another, so they can’t combine forces to make a specific region really weak,” explains Emily, “however, low pH and low dissolved oxygen both target the adhesive plaque, so that combination could be particularly troublesome.”

Building on these results, Emily has developed a predictive model that estimates the likelihood of mussel mortality based on biomechanical theories and backed by her mussel byssal experiments. By modifying the model to change the environmental conditions in various ways, Emily is now able to further explore the relationship between biomechanics and mussel mortality in the context of future climate change.

“This provides mussel growers and resource managers with a tool for predicting which water conditions are harmful, which is the first step in developing monitoring and mitigation strategies,” she concludes.

DRAGONS IN DANGER…

Adult damselfly emerging. Photo: Nedim Tüzün

While there were plenty of talks concerning the effects of climate change on marine species, there were also a number of talks dealing with terrestrial and aerial animals too. Two such researchers presented their work on the relationships between climate change and biomechanics in two enigmatic groups of insects: dragonflies and damselflies.

Zak Mitchell, a postgraduate researcher at the University of Leeds, reported on his PhD work concerning the important link between the flight performance of dragonflies and the effects of climate change on their natural distribution. “Dragonflies are notoriously good fliers, but their development and life history are directly related to temperature” says Zak. “Previous work has shown that most dragonfly species are responding in some way to increasing global temperatures.” Dragonflies rely on their ability to fly for critically important aspects of their daily life such as hunting and escaping predators, but their long-term survival may also depend on their ability to move into new habitats when the climate shifts. Changing global temperatures are shifting the range margins of many plants and animals towards the planet’s poles³, but what does this mean for dragonfly species of differing flight capabilities and how can this research be best used to protect them?

To answer these questions, Zak drew on an impressive range of technical gadgets and historical data sources. Using a specially constructed mirror-cube flight arena and a high-speed camera, Zak was able to fly dragonflies and track their movements from multiple angles, which allowed him to create a digital 3D reconstruction of their flight patterns and measure their flight performance in terms of speed and manoeuvrability. In order to link this with the insects’ ecology, Zak scoured databases of British dragonfly sightings over the past 25 years to calculate the changes in range margins for 12 British dragonfly species. Together, Zak used these data sources to link their flight performance and their ecology and interpret what this could mean for dragonflies in the face of a shifting climate.

Zak’s work reveals that dragonfly flight performance is correlated with the historical range expansion of each species, suggesting that better flying species are more capable of reaching new regions, but that other factors, such as the availability of suitable habitat, also play important roles and may limit the true extent of range expansions. Zak also highlighted the inconsistent claims made by previous studies linking flight performance and climate-induced range expansion, explaining that a more cohesive approach is required in order to better understand the interactions between these fields. “Some studies do not specify how they determine flight performance or they simply employ morphological proxies and assume that longer wings are indicative of better flight performance,” he explains. “Flight performance is a complex quantity and cannot easily be described by any one metric.”

In a rapidly changing world, it is crucial that conservation efforts make the most of the available knowledge in order to put scarce resources to their best use, and this is certainly true of Zak’s work on flight performance in the context of insect conservation. “The location of future dragonfly reserves must be planned in relation to the ability of relevant species to reach them - and for species with poor flight performance, stepping stone habitats may be vital in allowing them to expand in the face of climate change,” concludes Zak.

…AND DAMSELS IN DISTRESS

Later in the afternoon, Nedim Tüzün, a researcher at KU Leuven in Belgium, spoke about his work with a close relative of the dragonflies. “Damselflies are excellent model organisms for climate change studies because both the larvae and the adult react strongly to changes in temperature,” explains Nedim. “These reactions can often be detected in their physiology, morphology, locomotor performance and life-history traits.” Nedim is specifically interested in the effects of climate change that are carried over from early life stages and manifest in the adult form. “For example, temperature increases during the damselfly larval stage can affect the flight performance of the adult,” he says, “but is this due to changes in the development of the wings or the f light muscles?”

Nedim set out to solve this question by monitoring the development of damselflies from larvae through to adulthood and assessing their eventual flight performance. In order to reflect real world temperature fluctuations, Nedim created a controlled outdoor ‘mesocosm’ experiment that contained aquatic tanks for the damselfly larvae to develop in. These tanks were kept either at ambient temperature or at 4°C above ambient to represent a predicted future temperature increase due to climate change. Once the adults had emerged, he assessed their flight performance in a ‘flight tube’ and took measurements of their muscle content and wing shape to determine how they had been affected by raised temperatures during their earlier life stages.

“We found that larvae exposed to higher temperatures during development became adults with worse flight performance,” says Nedim, specifying that this reduction in flight performance appeared to be linked to a reduced flight muscle mass observed in the adults from the heated mesocosms. “This demonstrates that the carry-over effects of warming during early life stages can bridge metamorphosis and negatively affect the ability of these insects to fly.” Since flight performance is a crucial aspect of feeding and dispersing for many airborne insects, this poses a problem for damsel survival in the predicted warmer climate of the future. However, Nedim suggests that there is hope: “French populations of the same damselfly, for example, perform better at higher temperatures compared to Swedish populations - simply because the French are exposed to, and consequently adapted to, higher temperatures.” But with the climate changing at an ever-increasing pace, will these damselflies be able to adapt rapidly enough, or will they simply struggle to acclimatise to the new warmer world? Only time will tell.

References:

1. Lefrançois C, Shingles A, Domenici P (2005) The effect of hypoxia on locomotor performance and behaviour during escape in the golden grey mullet (Liza aurata). J Fish Biol, 67, 1711-1729
2. https://www.fws.gov/midwest/endangered/clams/mussels.Html
3. Chen, I. C., Hill, J. K., Ohlemüller, R., Roy, D. B., & Thomas, C. D. (2011). Rapid range shifts

Watch out for a collection of articles from this session which are due to appear in the SEB’s journal Conservation Physiology: https://academic.oup.com/Conphys