It's all about performance

01 November 2017 - By: Caroline Wood

It's all about performance

Bar-headed goose
Bar-Headed Geese make one of the most demanding migrations known on earth Photo: Nyambayar Batbayar

By Caroline Wood

As wildlife documentaries show, many animals undertake astonishing feats in order to survive migrate or win themselves a mate. Even when it appears effortless, these behaviours are typically supported by a whole complex of intrinsic adaptations at the genetic, cellular, physiological and behavioural level. Around the world, research is slowly picking apart how these animal athletes interact with their environment, some of which is showcased here from the SEB Annual Meeting in Gothenburg.

Flying high

For humans, perhaps the ultimate challenge is to conquer Mount Everest, a feat that demands months of training and preparation. Yet, for Bar-headed Geese (Anser indicus) to make such an ascent, they can, quite literally, ‘wing it’. These birds perform one of the most demanding migrations on earth as they travel across the Tibetan plateau between their breeding grounds in Mongolia and China, and their wintering grounds in the Indian subcontinent. Paradoxically, flight is one of the most metabolically demanding forms of locomotion, yet these birds perform it in an extremely oxygen-poor environment. “The geese ascend to the highest part of their migration, which can be over 5,500 m in the Himalayas, in under 8 hours giving them no opportunity to acclimatise”, said Lucy Hawkes ( University of Exeter, United Kingdom).“In contrast, humans that arrive at Everest base camp at 5,400m struggle to sleep well and eat properly until they have acclimatised over several weeks”. Given that they have no time to adapt raises the question: do Bar-headed Geese need to undergo training before they are ready to migrate?

To investigate this possibility, Lucy and colleagues implanted logger devices into four wild Bar-headed Geese captured in Western Magnolia.“This allowed us to look for changes in heart rate that might indicate increased physiological fitness; a reduced heart rate, for instance, could indicate a higher stroke volume”, said Lucy. “The loggers also included accelerometers to measure activity, including intense, demanding activities such as ground-based flapping which might represent power training. You could call them a ‘Fit-Bit’ for geese!”

The results showed that, prior to migrating, the geese demonstrated no significant differences in heart rate or activity patterns. “The geese don’t seem overtly to prepare for migration, other than eating a lot more grass and putting on weight”, said Lucy. “From a human perspective, this is like running a marathon with ease, after never training at all – apart from the pre-race pasta party. It may also apply to other birds that make spectacular migrations, such as Arctic Terns, Bar-tailed Godwits and Great Snipe, but this has yet to be demonstrated.”

One possible explanation is that for migratory birds, endogenous muscle development can occur without the need for power training. This stems from the observation that migratory birds experience large fluctuations in muscle mass each year: muscle is consumed to fuel their long journeys and rebuilt again during their stopovers in wintering and breeding grounds. As an example, Barnacle Geese lose approximately a third of their flight muscle mass when they moult their wing feathers. But in studies where Barnacle Geese were kept captive, deprived of the ability to fly freely, their wing muscles still regrew to pre-moult levels1 suggesting that muscle development is regulated by other mechanisms, rather than activity levels. It has been hypothesised that changing photoperiods could trigger the release of hormones that upregulate genetic pathways for muscle growth and fuel mobilisation. In support of this, White-Throated Sparrows (Zonotrichia albicollis) have been found to increase gene expression of Fatty Acid Binding Proteins (FABPs) and Fatty Acid Translocase proteins by 1000% during their migratory season: proteins that are critical for transporting fatty acids through the muscle membrane2.

Surely it must be every bodybuilder’s dream to unlock the secret of bulking up their muscles without spending hours in the gym…but as for Lucy, she is already getting ready for her next line of enquiry: “We are now investigating how geese deal with the temperature changes they experience during migration, from extremely cold air in the Himalayas to extremely warm air down in India, all whilst wearing the equivalent of a duvet!”, she said. 

Diving Deep

It’s not just up high where we see incredible animal performances, other creatures are capable of plunging down to the ocean depths, seemingly without harm. In mammals, the current record for the deepest dive belongs to a Cuvier’s Beaked Whale (Ziphius cavirostris), which has been recorded diving to a depth of 2992 m, during a 137-minute dive3. In comparison, the current record for a human free-diver is merely 121 m in a dive lasting four minutes and 24 seconds4. One of the key reasons behind this difference is the incredible resilience of diving mammals to hypoxia, particularly in the brain, as Andrej Fabrizius (Institute of Zoology, University of Hamburg, Germany) explained: “In most terrestrial mammals, lack of oxygen results in irreversible damage to the brain in a few minutes, but the brains of diving mammals can survive recurrent and extended periods of hypoxia”.

The brain is particularly vulnerable to damage from hypoxia due to its high metabolic activity, which requires a constant supply of oxygen. In humans, for instance, the brain comprises only 2% of our body weight yet accounts for 20% of the body’s oxygen demand. Many physiological and anatomical adaptations that increase oxygen delivery to the brain in diving whales and seals are already known, including increased blood volumes, high levels of haemoglobin and myoglobin, and constriction of blood vessels to peripheral areas during dives. But the cellular and molecular mechanisms that protect against hypoxia remain largely unknown.  
Hooded seals have been recorded diving down to depths of over 1000m. Photo:

To investigate this, Andrej took brain tissue samples from the visual cortex of the Hooded Seal (Cystophora cristata), a species which has been recorded diving for up to an hour and reaching depths of over 1000 m. These were compared with visual cortex samples from ferrets, the closest terrestrial relative to Pinnipeds (seals and walruses), having diverged 38-40 million years ago. “We used RNA-sequencing analysis as a first ‘shot in the dark’ to see if we could find any genes showing significant differences in regulation between seals and ferrets”, said Andrej5. The results showed no evidence of enrichment for enzymes relating to anaerobic respiration, such as lactate dehydrogenase, in the seal brains. However, genes relating to aerobic energy metabolism and translation (the production of proteins from amino acids) were significantly overrepresented in the ferret brain. “This suggests that, rather than having a higher anaerobic capacity, the seal brain may be adapted to low oxygen conditions by having a lower aerobic energy metabolism which would reduce the energy demand”, said Andrej.  

Besides this, two other genes showed unusually high expression in the seal brain, making them potential candidates for a hypoxia-adapted mechanism. The most highly expressed gene, clusterin, is thought to interfere with programmed cell death (apoptosis), thus promoting cell survival. “The high level of clusterin in the seal brain could be interpreted either as a pre-adaptation to protect it from damage or as a consequence of the hypoxic conditions encountered during a dive”, said Andrej. Interestingly, in humans clusterin is thought to prevent the build-up of amyloid-β plaques that are the hallmarks of Alzheimer’s disease. The gene with the largest difference in expression between seals and ferrets was S100B, a calcium-binding protein that regulates a number of processes, including the activation of astrocytes (cells which support the function of the central nervous system) following brain damage. “Interestingly, when we compared our results with brain transcriptomes of other mammals, we also found high S100B expression in Minke and Bowhead whales, but low expression in terrestrial mammals”, said Andrej. “Therefore, S100B could be a component of a common adaptation mechanism that evolved convergently in whales and seals.” Besides uncovering the secrets of these extraordinary divers, Andrej hopes that his results could also have applications for land-locked humans: “Millions of individuals die or become ill each year as a result of diseases that reduce the blood supply to oxygen sensitive tissues, such as strokes”, he said. “Potentially, clusterin and S100B could be suitable targets for drug therapies to treat these conditions”.

Meet the new neighbours

Perhaps one of the greatest impacts on successful performance is the sudden arrival of an exotic, superior competitor. Across the globe, there are countless examples of introduced invasive species competing directly with the natives, often with devastating consequences. Take the American Signal Crayfish, for instance, introduced into Europe in the 1960s, partly through farming for the restaurant trade. Larger and more aggressive than native European White-clawed Crayfish, the Signal Crayfish monopolises food resources and shelter, besides transmitting a fungus that is deadly against the White-clawed Crayfish6. In cases such as these, it is inevitable that the subordinate, native species will be outcompeted.

But recent research indicates that invasive species can exert much more subtle influences as well, even when they do not appear to challenge native species.  “In the absence of direct competition or predation pressure, invasive species can still affect populations of native species, for example by influencing environmental complexity and stochasticity”, said Jörgen Johnsson (University of Gothenburg, Sweden). His studies have focused on the interaction between native Brown Trout (Salmo trutta) and invasive Brook Trout (Salvelinus fontinalis); a species introduced in early 1900s to enhance sport fishing. “Previous studies have shown that Brook Trout have negative effects on growth, survival and reproduction of Brown Trout, but the mechanism is not well understood, as the ecological niches of these species have previously been found to be partly segregated”, said Jörgen. “In addition, Brown Trout tends to dominate Brook Trout in direct interactions.”
Brook Trout
The Brown Trout – a native species threatened by invasive Brook Trout. Photo: Bart Adriaenssens

One hypothesis is that invasive species can break down adaptive phenotypic syndromes, where functionally related traits show patterns of variation. In fish, for instance, territorial individuals are typically aggressive, highly active and have high metabolic rates.  “Potentially, novel selection pressures induced by the non-native species break down the associations among phenotypic traits in the native species”, said Jörgen. To investigate this, Jörgen and his colleagues compared groups of Brown Trout living either alone or together with Brook Trout in a stretch of Ringsbacken, a small stream in southern Sweden. Besides measuring physical traits such as body length and mass, the fish were also fitted with electronic tags so that their activity levels could be recorded. Fin samples were also subjected to isotope analyses to estimate each fish’s dietary composition. “Our study is the first to integrate morphological, behavioural and physiological traits in a lab setting with performance in the wild to investigate the influence of non-native species”, said Jörgen. 

The results showed that “integration of phenotypic traits was substantially reduced when Brown Trout live with Brook Trout” said Jörgen7. “Whereas before, we saw strong relationships between, for instance, metabolic rate and activity, in the presence of Brook Trout there was almost no association between these traits”. The trout showing such trait dissociation also had reduced growth rates, a proxy for fitness, underlining how the integration of related traits has adaptive value. Furthermore, Brown Trout living with Brook Trout showed a shifted ecological niche, with smaller home ranges, stouter body shapes and a higher proportion of terrestrial prey (e.g. earthworms that fall into the stream). 

If the Brook Trout are not directly competing with the Brown Trout, how are they exerting these effects? Jörgen speculates that they may disrupt circadian feeding patterns in the native species: “Preliminary results suggest that the presence of Brook Trout alters activity patterns in Brown Trout: from being mainly nocturnal, they start to become more active during the day, shifting to the temporal pattern of the Brook Trout. There may also be social information being exchanged between the species, particularly at the younger stages when they appear very similar morphologically”.

Potentially, “breakdown of adaptive phenotypic syndromes may help explain other deleterious effects of non-native species in the absence of direct competition with the native species” Jörgen concludes. 

The high cost of sex  

Sometimes it is not invasive species that are the main worry, but members of your own species – particularly during the mating season. Black Grouse, for example, perform some of the most energetic behaviours in their bid to win females. “Grouse are very much like decathletes in that they have to excel at a whole composite of different behaviours, known as ‘lekking’”, said Carl Soulsbury (University of Lincoln, United Kingdom). This includes long-distance calls, rookoing (vibrating their air sacs), holding their tail fans erect, vertically leaping 2-3 feet into the air, beating their wings and brutal fights. “They look like little wind-up toys as they are always on the go. It’s a good example of multiple sexual signals from both phenotype and behaviour providing information about male quality”, said Carl.  

On the largest leks, up to 50 male grouse congregate at traditional grounds each year, where they attempt to defend a small territory: the closer this is to the centre of the lek, the more attractive they are to females. “It’s a system driven entirely by female choice, so it is very skewed towards exceptional males”, said Carl. “Typically, one male will dominate and, across their entire lives, more than half of the males will never mate at all”. But these incredible displays come at a high price: lekking males typically lose 12-20% of their body mass and, of those that do reproduce successfully, nearly three quarters subsequently die. As a result, grouse are relatively short-lived compared with most bird species, with few surviving beyond four years.
Black Grouse
Black Grouse perform some of the most energetically costly behaviours known in their bid to win a mate. Photo: Gilbert Ludwig

Given that they may only have one shot at success, timing is critical. Most male grouse start lekking in their second year, with only a handful attempting it in their first year. But how do the grouse decide when to enter the battle arena? “That decision is complex”, said Carl. “Ultimately, we think it is a combination of both internal factors, such as parasite load and immunity, and external factors, including population density. But we don’t know the balance of these”. 

As part of a project that has been observing grouse at traditional lekking sites in Central Finland over 15 years, Carl and his colleagues are starting to put together the pieces of the puzzle. “We know that when the population is higher, the poorer quality males start lekking earlier” he said. “This could be due to there being fewer older, heavier males in relation to yearling males when populations are increasing”.  

Curiously, it appears that the grouse also have a sense of whether they are likely to survive until the next year’s lek. “As they enter their final year, male grouse often develop black spots on the tips of the their white undertail feathers”, said Carl. “Males also increase their lekking effort– a phenomenon we call ‘terminal investment’”. It is thought that the white tail fan plays an important role in female choice, as previous studies which experimentally cut these feathers found that this reduced male mating success8. Possibly, the black spots are similarly interpreted as a sign of damage, as Carl explained: “It takes active effort and control for a male grouse to produce white feathers, so the appearance of black spots is clearly an indication that something is wrong at the physiological level. Oxidative stress or a deficiency of antioxidants may be involved, but at this stage we don’t know the cause. Yet these birds seem to understand some aspect of this, and that drives them to invest in their final lekking attempt”. 

“In the future, we hope to characterise the fitness costs of lekking behaviour and link this with the genetic and epigenetic underpinnings of sexual traits” said Carl. “As more techniques develop, there are more questions we can ask. As an example, we hope to use comet assays in the future to assess the role of DNA damage in aging for these birds”. 

Clearly, extraordinary performances in the animal world are the result of complex factors responding to ever-changing and extreme environmental theatres. Research is only just beginning to unravel these mechanisms to help us to understand how these animal actors perform, as well as giving us insights into how we could exploit this new knowledge.

1. Portugal, Steven J., et al. "Testing the use/disuse hypothesis: pectoral and leg muscle changes in captive barnacle geese Brantaleucopsis during wing moult." Journal of Experimental Biology 212.15 (2009): 2403-2410.
2. McFarlan, Jay T., ArendBonen, and Christopher G. Guglielmo. "Seasonal upregulation of fatty acid transporters in flight muscles of migratory white-throated sparrows (Zonotrichiaalbicollis)." Journal of Experimental Biology 212.18 (2009): 2934-2940.
3.Schorr, Gregory S., et al. "First long-term behavioral records from Cuvier’s beaked whales (Ziphiuscavirostris) reveal record-breaking dives." PloS one 9.3 (2014): e92633.
4.Freediving world record set by William Trubridge with 122m dive. The Guardian, 02/05/2016.
5.Fabrizius, Andrej, et al. "When the brain goes diving: transcriptome analysis reveals a reduced aerobic energy metabolism and increased stress proteins in the seal brain." BMC genomics 17.1 (2016): 583.
6. Invasive Crayfish Species. Published by The Environment Agency and Buglife :
7. Závorka, Libor, et al. "Co-existence with non-native brook trout breaks down the integration of phenotypic traits in brown trout parr." Functional Ecology (2017).
8.Höglund, Jacob, et al. "Context-dependent effects of tail-ornament damage on mating success in black grouse." Behavioral Ecology 5.2 (1994): 182-187.




Category: SEB Gothenburg 2017
Caroline Wood-Author Profile

Caroline Wood

Caroline Wood was the SEB’s 2014 science communication intern. Since then, Caroline has been a regular contributor the SEB, reporting on events and writing insightful features for our members.
Caroline has an undergraduate degree from Durham University in Cell Biology and is currently a PHD student at Sheffield University studying parasitic Striga weeds that infect food crops. You can read her blog here.


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