Comparative Biochemistry and Physiology, Part A 156 (2010) 301302

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Comparative Biochemistry and Physiology, Part A

j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / c b p a

Preface

Breathing, locomotion and everything in-between

Respiration and locomotion are fundamental processes for

animals. Understanding how these systems function in the face of
different constraints; biological, mechanical and physiological, was
highlighted during a one day symposium entitled Breathing,
Locomotion and Everything In-between held from August 913,
2009 at the 2nd International Congress of Respiratory Science (ICRS,
www.respiratory-science.org). The ICRS was held in the spa town of
Bad Honnef near Bonn, Germany. The ICRS meetings were the
brainchild of Prof S.F. Perry and fullled a long held desire of his to
bring together researchers covering the enormous breadth and
potential of the Respiratory Science discipline in one place. The ICRS
has been successful in formulating a truly cross-disciplinary approach,
bridging traditional barriers and fostering networking opportunities
from molecules to ecosystems. This volume contains a selection of the
papers presented at the symposium.
During the evolution of aspiration ventilation, the hypobranchial
system was gradually replaced by the axial musculoskeletal system in
lung ventilation. First exhalation then inspiration was facilitated by
the axial muscles, at the branch points of the Tetrapoda and Amniota,
respectively. This shift allowed the development of diverse feeding
mechanisms by freeing the tongue and head but also generated a
conict between the ventilatory and locomotor systems resulting in
mechanical constraints. Like all animals birds must expend energy in
order to move around. The evolution of intense locomotor activity
required a respiratory system that was highly effective at meeting
these energetic demands. This necessitated a functional link between
the respiratory and locomotor systems: respiration powers locomotion. Examining the complexities of how birds breathe, the cost of
terrestrial locomotion and their adaptations to extreme environments
were the focus of four papers presented during the symposium.
The morphology, physiology and function(s) of avian accessory
breathing structures, the uncinate processes, were reviewed (Codd, in
press). Ossied uncinate processes are present in almost all extant
birds and also occur in extinct forms (early tetrapods, amphibians and
some non-avian dinosaurs). Uncinate processes extend from the
midpoint of the vertebral ribs and can be either ossied to or
cartilaginously attached to the following vertebral rib. These processes are integral to the breathing mechanics of birds being involved in
inspiration, expiration and locomotion. Perhaps the most striking
nding from this research is that adaptations to different forms of
locomotion (walking/running, swimming, ying, and diving) appear
to be the driver behind morphological adaptations in these processes.
Uncinate processes are also found in the fossil record and represent
another characteristic linking modern birds to their theropod
dinosaur ancestors.
The energetics of locomotion in barnacle geese (Branta leucopsis)
were examined in two papers by Tickle et al. (in press) and Nudds
1095-6433/$ see front matter 2010 Elsevier Inc. All rights reserved.
doi:10.1016/j.cbpa.2010.03.010

et al. (in press). Birds must balance their energy budgets and despite
having an extremely efcient respiratory system they incur high
energetic costs during locomotion. Recently interest has been
reviewed in avian energetics by the nding that birds can be
distinguished by adaptations to different locomotor modes (Tickle
et al., 2007). Examining birds from these different groups sheds new
light on the cost of locomotion in birds. B. leucopsis are classied as
non-specialists meaning they are able to walk, swim and y and likely
to have a compromised morphology for any particular locomotor
mode. During bipedal locomotion birds are thought to use gait
changes to minimise the costs of locomotion. However, Nudds et al.
(in press) demonstrated that this is not always the case. Unlike other
species of birds that waddle when walking, no evidence for an aerial
phase was found during treadmill locomotion of B. leucopsis. Being
non-specialists B. leucopsis are a morphological compromise between
a bird adapted to swim, y or walk and it appears that this
compromise has lead them to be relatively inefcient walkers.
Continuing investigations into constraints on animal morphology
Tickle et al. (in press) examined the energetics of load carrying in
B. leucopsis. The application of loads has been widely used to
understand cost of locomotion and has revealed some extraordinary
physiological adaptations from humans to insects. B. leucopsis are able
to carry loads more efciently than mammals, however the placement
of the load has a signicant effect on the cost. Load carried on the back
elicit a directly proportional increase in metabolic rate, however loads
carried on the sternum and legs incur proportionally greater costs.
Sternal loads are twice as expensive as back loads to carry while any
load on the limb is more costly again. These ndings may shed new
light on the cost of breathing in bird's as any additional mass added to
the sternum must be moved up and down with each breath. For
example, it would be intriguing to examine if the addition of loads
resulted in the recruitment of novel hypaxial muscles to facilitate
breathing and/or locomotion.
There are more than 10,000 species of bird and as a group they
demonstrate an incredible range of adaptations. However, compared to
other vertebrates, birds are capable of intense, energetically expensive
periods of activity. There are birds specialised to dive, swim and run for
example. However, all extant avian species evolved from volant
ancestors and during ight the metabolic rate of birds can increase by
over 23 times the maximum values of similar sized mammals and
oxygen uptake of some ying birds increases by up to 20 times that of
resting birds. Flight is an energetically expensive form of locomotion
however there are birds capable of long distance polar migrations
and peregrine falcons can achieve speeds of over 400 km/h during
swooping. Perhaps the most remarkable feat, however, is the migration
of bar headed geese ying at altitudes of between 5 and 9000 m as they
migrate across the Himalayas. Flying at these altitudes means these

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Preface

birds are exchanging gas where the partial pressure of oxygen is about
one third that at sea level. Bar headed geese have a suite of adaptations
that facilitate breathing and locomotion under these extreme conditions
(Butler, in press). Key adaptations appear to be changes in blood
chemistry that enable a greater carrying capacity of haemoglobin, and
the ability to tolerate large increases in breathing frequency during
periods of low oxygen when compared to mammals. Despite these
physiological changes, an intriguing new idea (Butler, in press) suggests
that behavioural adaptations may also play a key role. Butler and
colleagues are currently testing hypotheses that these birds are able to
make use to slope soaring as a further way of reducing the metabolic
costs. This idea may provide an explanation for how these birds are able
to y to such heights whilst experiencing such challenges to maintaining effective gas exchange.
Understanding adaptations often requires novel and somewhat
complicated approaches. Much can be learnt however from detailed
investigations of animal anatomy and morphology. A detailed
investigation of the morphology of the respiratory system in the
Testudines (Lambertz et al., in press) provides a good case in point. In
mammals, archosaurs and some lepidosaurs the post pulmonary
septum (PPS), together with the post hepatic septum (PHS), are some
of the most important intracoloemic membranes. By examining lung
structure and coloemic organisation in detail Lambertz et al. were able
to show that all of the major Testudine taxa posses a post pulmonary
septum. Findings such as these can be invaluable in attempts to
reconstruct phylogenetic relationships and provide new information
on the evolution of accessory breathing structures across vertebrate
groups.
One of the central themes of the ICRS meetings is the removal of
traditional barriers to cross-disciplinary research. Our symposium
benetted greatly from this approach and meant participants were
able to see research in areas outside of their own areas. Research
presented by Lehmann and Cierotzki (in press) on the locomotor
performance of Drosophila mutant highlighted the benets of a
diverse symposium. Classically constraints of breathing and locomotion are thought to only apply to vertebrates groups however,
invertebrates must also move and breathe efciently. The drop-dead
mutant strain of Drosophila suffers from dysfunction in their
respiratory system that manifests as a reduction in tracheal oxygen
supply. Surprisingly these ies are more active and motivated to run

than the wild type suggesting that plasticity in breathing and

locomotion are common themes in the animal world.
In closing we would like to thank the many authors who
contributed in making the symposium such a success. We would
also like to acknowledge the nancial support provided for the ICRS by
Sable Systems International, Sable Systems Europe, Qubit Systems,
Loligo Systems, Karger Publishing, the Deutsche Forschunggemeinschaft, Morphisto and Nima Technologies.
References
Butler, P.J., in press. High iers: the physiology of bar-headed geese. Comp. Biochem.
Physiol. A. doi:10.1016/j.cbpa.2010.01.016.
Codd, J.R., in press. Uncinate processes in birds: morphology, physiology and function.
Comp. Biochem. Physiol. A. doi:10.1016/j.cbpa.2010.02.010.
Lambertz, M., Bhme, W., Perry, S. F., in press. The anatomy of the respiratory system in
Platysternon megacephalum Gray, 1831 (Testudines: Cryptodira) and related species,
and its phylogenetic implications. Comp. Biochem. Physiol. A. doi:10.1016/j.
cbpa.2009.12.016.
Lehmann, F.-O., Cierotzki V., in press. Locomotor performance in the Drosophila brain
mutant drop-dead. Comp. Biochem. Physiol. A. doi:10.1016/j.cbpa/2009.12.019.
Nudds, R.L., Gardiner, J.D., Tickle, P.G., Codd, J.R., in press. Energetics and kinematics of
walking in the barnacle goose (Branta leucopsis). Comp. Biochem. Physiol. A.
doi:10.1016/j.cbpa.2010.01.023.
Tickle, P.G., Ennos, A.R., Lennox, L.E., Perry, S.F., Codd, J.R., 2007. Functional signicance
of the uncinate processes in birds. J. Exp. Biol. 210, 39553961.
Tickle, P.G., Richardson, M.F., Codd, J.R., in press. Load carrying during locomotion in the
barnacle goose (Branta leucopsis): the effect of load placement and size. Comp.
Biochem. Physiol. A. doi:10.1016/j.cbpa.2010.01.022.

Jonathan R. Codd
Faculty of Life Sciences, University of Manchester,
Manchester M13 9PT, UK
Corresponding author. Tel.: +44 161 275 5474.
E-mail address: jonathan.codd@manchester.ac.uk.
Wilfried Klein
Instituto de Biologia, Universidade Federal da Bahia,
Salvador, Bahia, Brazil
Corresponding author. Tel.: +55 71 328 36560.
E-mail address: klein@ufba.br.