The Little Feathered Ecosystem Engineer

OUTSIDE JEB

The little feathered marine-derived nutrients in the form of vital that we understand which animals nitrogen and carbon stable isotopes. are significant ecosystem engineers in ecosystem engineer These samples came from a wide range of order to conserve habitats and protect sources, including soil, algae, scats and biodiversity. fur. In addition, the researchers also tracked the flight paths of a number of 10.1242/jeb.147397 little auks, as the birds also distribute González-Bergonzoni, I., Johansen, K. L., nutrients via their droppings during their Mosbech, A., Landkildehus, F., Jeppesen, E. foraging trips. The team found a huge and Davidson, T. A. (2017). Small birds, big effects: the little auk (Alle alle) transforms high increase in marine-derived nitrogen arctic ecosystems. Proc. R. Soc. B 284, 20162572. levels, almost 10-fold, in the terrestrial and freshwater samples from colony sites Clare Stawski University of New England as well as the associated flight paths; this [email protected] is greater than the nitrogen transfer

ECOLOGY provided by fish. However, the levels of All animals have an effect on the marine-derived carbon only increased in environment, but some key species – the freshwater ecosystems and not in Lateralisation helps called ecosystem engineers – can have a terrestrial areas. particularly large influence. Their impact sailfish snatch sardines can be positive, by creating and Next, to determine the effect of the maintaining habitats and increasing additional nutrient load, the team biodiversity, but they can also be measured the species richness and negative, by destroying habitats and physical–chemical characteristics of reducing biodiversity. Interestingly, the freshwater communities while also magnitude of the effect that an ecosystem measuring the species richness and the engineer has on the environment is often productivity of the vegetation in the not a reflection of their size. Some are terrestrial habitats, which allowed them to huge, such as elephants, which provide quantify what the increase in nitrogen water for other animals during the dry levels actually means for the ecosystems. season by digging up desiccated water The higher nutrient levels at little auk sites holes until water flows. But others are and flight paths contributed to an PREDATION tiny, such as plankton in the oceans, increased algal biomass in the freshwater When we pick up a pen to write, we tend to which influence the amount of light ecosystems and increased vegetation in use either our right or our left hand. This reaching the plants down below. In the terrestrial areas, suggesting much lateralisation helps us react rapidly and cuts particular, the transportation of marine- better primary productivity as a result of down on how much nerve tissue we need. derived nutrients by animals is vital in these small birds. In addition, many more But if you are a predator, lateralisation may shaping not only oceans but also animals, such as hares and muskoxen, be costly: if prey can anticipate your angle freshwater and terrestrial ecosystems. were seen at terrestrial sites near the of attack, it may help them escape. This Ivan González-Bergonzoni from the colonies, in contrast to the more barren predictability might select against Universidad de la República, Uruguay, areas that were not colonised by the little lateralisation in predatory species. and his international team of researchers auks. Conversely, the team found that the However, Ralf Kurvers from the Center for decided to observe this phenomenon from species richness in the freshwater Adaptive Rationality in Berlin, and an a seabird’s perspective. ecosystems near little auk colonies was international team of collaborators reduced, probably because of the increase suspected that group-hunting sailfish, The seabird in question is the little auk in water acidity and the algae that Istiophorus platypterus, might have the best (Alle alle), which constitutes the largest flourished as a result of nutrient of both worlds. As sailfish attack schools of population of seabirds in the North enrichment. sardines by slashing and tapping their prey Atlantic region, where they consume with elongated bills, the team wondered enormous amounts of zooplankton on a González-Bergonzoni and his group have whether the communal fish might dodge daily basis. The team travelled to the unequivocally shown that a single tiny the costs of lateralisation while exploiting North Water Polynya between Northwest bird species, the little auk, has a massive its benefits by hunting in a pack, where, Greenland and Canada, which is home to impact on the habitats of the North Water despite individual-level lateralisation, 60–70 million breeding pairs, to collect Polynya. By shaping these environments, attacks still come from all angles. samples from terrestrial and freshwater the little auk is truly an ecosystem habitats at sites with and without colonies engineer and its loss would probably Snorkelling off the coast of Cancun in in order to measure the content of result in a very different landscape. It is Mexico, the researchers filmed wild sailfish

Outside JEB is a monthly feature that reports the most exciting developments in experimental biology. Articles that have been selected and written by a team of active research scientists highlight the papers that JEB readers can’t afford to miss. Journal of Experimental Biology

1934 OUTSIDE JEB Journal of Experimental Biology (2017) 220, 1934-1936 huntingandanalysedthemoviesbackinthe evolution of lateralization in group hunting sailfish. meaning 150 trillion kilograms of Curr. Biol. lab. The team then identified individual 27, 521-526. oxygen have disappeared from the sailfish using each fish’s unique dorsal fin C. Ruth Archer World Ocean over the past 50 years. This morphology and found that sailfish University of Exeter begged two questions: how were consistently attack from either the right or [email protected] these changes distributed throughout the left, suggesting that the fish demonstrate the ocean?; and where did all the lateralisation. Knowing that the fish appear oxygen go? to favour one side over the other, the team Oceans of oxygen, gone suspected that the teeth lining the dominant The team set about answering the first side of the fish’s bills would be more question by directing their analyses abraded, in much the same way that humans towards particular ocean basins. All 10 are more likely to injure their dominant basins they examined lost oxygen, but hand. To test this idea, they compared the some lost more than others. The largest condition of micro-teeth in sailfish bills and fraction of oxygen (∼40%) was lost in found that tooth abrasion was always more the North and Equatorial Pacific, pronounced on one side or the other. while the smallest fraction (∼1%) was Together, this behavioural and lost in the North Atlantic. Interestingly, morphological evidence points to the team found that the rapidly changing lateralisation in individual sailfish. Arctic Ocean swung well above its

OXYGEN DEPLETION weight class in terms of its contribution So, if sailfish are lateralised, does this ‘Hypoxia’ is a well-used word among to oxygen depletion: 7.6% of the total reduce their hunting success by helping JEB authors. These past 10 years have lost oxygen despite containing a meagre sardines to pre-empt their angle of attack? seen it used in over 80 titles, 200 1.2% of the world’s seawater. Perhaps The team answered this question by abstracts and 800 articles, which means most unsettling, the World Ocean’s seeing how the strength of lateralisation in great effort is being put towards anoxic regions have quadrupled in size each sailfish correlated with its sardine understanding the physiological since 1960. capture success. The result was clear: responses of animals to low oxygen. increased lateralisation promotes hunting Good thing, because rising atmospheric As for where all the oxygen went, the success and sailfish are more likely to temperatures are making the Earth’s team’s prime suspect was reduced successfully snatch a sardine if attacking aquatic habitats more hypoxic. Sunke oxygen solubility; as rising atmospheric from their preferred side. Schmidtko and his team at GEOMAR’s temperatures drag world oceanic Helmholtz Centre for Ocean Research in temperatures up with them, less oxygen Given that lateralisation often incurs costs Kiel, Germany, were familiar with the is able to dissolve into the seawater, for predators, how does this trait help biotic and abiotic theories underlying owing to water’s physicochemical sailfish on the hunt? The team suspected this trend, but decided to quantify just properties. The team combed through that group hunting could reduce the costs of how much oxygen the World Ocean has their temperature data and found that lateralisation if hunting groups contain a lost in recent years. reduced oxygen solubility did indeed mix of right- and left-billed sailfish. To test play a role – particularly in the ocean’s this idea, the team randomly selected The Kiel team isn’t the first to inventory uppermost 1000 m – but only accounted individuals that they observed hunting at the World Ocean for oxygen, but they for 15% of all oxygen lost. To account least three times, and put them together into certainly went farther and deeper than for the other 85%, the team suspected random groups that varied in size from 1 to anyone before. They started by locating biological and chemical patterns of 15 fish. They calculated how lateralised five publicly accessible databases from oxygen consumption in combination these groups were by averaging the mean the likes of NOAA and Pangaea and with complex ocean ventilation laterality of each of the group members. As then used these to piece together an dynamics. These processes are each the hunting groups increased in size, the elaborate profile of oceanic oxygen at influenced by climate variability in ways overall degree of lateralisation across the 78 depth levels over the past 50 years. that could theoretically explain the Kiel entire group declined. That is, although This more than quadrupled the volume team’s results, but future studies will be individuals may be lateralised, the net of water previously analysed for oxygen needed to address these hypotheses lateralisation of the group is reduced as the and allowed them to paint a detailed directly. number of left-lateralised fish cancels out picture of how the past 50 years has the number of right-lateralised animals. So, affected the World Ocean’s oxygen So, the world ocean is definitely hunting in a group provides the unexpected content. Perhaps unsurprisingly, they becoming more hypoxic, impacting the benefit of allowing individual predators to have not been kind. marine ecosystem as a whole in ways exploit the benefits of lateralisation, while that are complex and, in many cases, their prey still have no idea which direction From the broadest perspective, Schmidtko not good. It also means that there the next attack is coming from. and his colleagues found that the World will be plenty of work for those 10.1242/jeb.147389 Ocean currently contains around researchers publishing on the hypoxic 227 petamol (1015 mol) of oxygen. That’s adaptations of animals, keeping them Kurvers, R. H., Krause, S., Viblanc, P. E., Herbert- a lot of oxygen – over seven quadrillion busy for years to come as we attempt to Read, J. E., Zaslansky, P., Domenici, P., Marras, S., Steffensen, J. F., Svendsen, kilograms of the stuff – but it’s about get to grips with this complex

M. B. S., Wilson, A. D. M. et al. (2017). The 4.8 petamol less than it was in 1960, ecological calamity. Journal of Experimental Biology

1935 OUTSIDE JEB Journal of Experimental Biology (2017) 220, 1934-1936

10.1242/jeb.147405 animal’s environment may more directly immobilised chicks grew shorter and Schmidtko, S., Stramma, L. and Visbeck, M. control development. disproportioned limbs. The researchers also (2017). Decline in global oceanic oxygen content ’ during the past five decades. Nature 542, took snapshots of the birds development 335-339. To investigate the immediate impact that over time and they saw that different environment, particularly temperature, parts of the limb were more sensitive to Matthew D. Regan University of British Columbia has on limb morphology, Andrea Pollard muscle paralysis at different times. [email protected] from the Royal Veterinary College, UK, and her colleagues studied the In the final leg of their experiments, the development of dwarf crocodiles. They team used molecular techniques to observed that crocodiles incubated at understand how movement is conveyed Fidgety embryos grow 32°C had longer limbs than their siblings to the developing bones. They saw that longer limbs developing at 28°C (even relative to their cell division in specific growth zones – larger total body size). More interesting ‘growth plates’–was slowed in the still, the two groups had differently immobilised chicks. They also looked at proportioned limbs: the warmer animals gene expression in the nascent limbs, had longer tibiae (corresponding to the which was particularly rewarding during human shinbone) but short toes, whilst the critical periods when immobilisation ‘ the cooler animals possessed paddle- had differing effects on growth in ’ like limbs with elongated toes. The different parts of the limb. During one authors hypothesise that the differences period, 58 genes were differentially may equip animals for better locomotor expressed in the femur, in which performance in their respective immobilisation affected development, environments after hatching, as the fossil compared with the tibiotarsus (the avian record intriguingly suggests that highly equivalent of the tibia), which was not DEVELOPMENT – aquatic crocodilian ancestors with more affected by muscle inhibition. They – The great evolutionary biologist Leigh paddle-like limbs inhabited cool additionally saw that several genes van Valen famously quipped: ‘Evolution temperate climates whereas extinct associated with cell contraction were – is the control of development by ecology’. equatorial species with longer legs but downregulated in the chicks that had – This aphorism neatly portrays how natural shorter toes were terrestrial. But how been immobilised. selection, over generations, sculpts could temperature have such a specific organism development and results in the effect on limb development? The clue This intriguing new study demonstrates that wonderful diversity of form exhibited in came from observing embryo activity; embryonic development is not just a the animal kingdom. Nowhere is this more those incubated at higher temperature passive result of historical natural selection; – obvious than limb morphology from made more frequent spontaneous development can be directly influenced by – wings to fins in vertebrates. But van movements within the egg. environment, and animals may be active Valen never imagined the process of architects of their own anatomy. development being directly manipulated Pollard and her colleagues had identified a by an organism’s environment. By and tantalising correlation between embryonic 10.1242/jeb.147413 large, development is controlled by movement and limb development, but to genetics, so the most obvious variations in provide an unequivocal link between the Pollard, A. S., Charlton, B. G., Hutchinson, J. R., limb anatomy between different species two they had to move to a more convenient Gustafsson, T., McGonnell, I. M., Timmons, J. A. and Pitsillides, A. A. (2017). Limb are encoded in the genome. However, organism to investigate: developing proportions show developmental plasticity in limb morphology also exhibits substantial chicken embryos in eggs. The team was response to embryo movement. Sci. Rep. 7, variation within individuals of the same able to suppress the chick’s limb movement 41926. species, especially when development with a drug that paralyses muscle William Joyce takes place in different conditions. This contraction. Just like the less active Aarhus University suggests that, beyond the genome, an crocodiles at low temperature, the [email protected] Journal of Experimental Biology

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