Winner of the 2014 Journal of Zoology ‘Paper of the Year’ award

18 06 2015

Seeing through the skin: dermal light sensitivity provides cryptism in moorish gecko

D. Fulgione, M. Trapanese, V. Maselli, D. Rippa, F. Itri, B. Avallone, R. Van Damme, D. M. Monti, and P. Raia

The ability of some animals to rapidly change colour fascinates and astounds us in equal measure. Such colour change is enabled by specialized cells called melanophores in the animal’s skin, and this phenomenon has been observed for instance in octopuses, chameleons and fiddler crabs. This ability allows the animal to use its colour as camouflage and blend into their background that is heterogeneous or constantly changing, in order to conceal it from its predators or prey. However, the mechanisms by which animals perceive their surroundings to match their colour to the background are still not clear.

Moorish geckos Tarentola mauritanica are known to turn darker or lighter depending on the tone of their surroundings, and Domenico Fulgione and his co-authors from University of Naples Federico II and University of Antwerp wanted to examine whether these geckos match their skin tone to their surroundings via the nervous system, endocrine system or local cell response. In order to test this, the authors brought wild-caught moorish geckos into the lab and as treatments covered their eyes or their trunk, and then put them inside terrariums covered by either black or white paper and with a transparent lid. The team then observed whether the geckos were still able to change their colour to match the tone of their surroundings.

Surprisingly, the blindfolded individuals still changed their colour consistently with their background, whereas when the geckos had their trunk covered they did not change colour, even when they could see their surroundings. This and examinations of opsin levels in tissue samples from various parts of the geckos’ body led the authors to conclude that the moorish geckos have melanophores on their trunk that are light-sensitive and react to the light reflectance levels of their surroundings, leading to the observed skin colour change. Although a similar phenomenon has been observed in some non-amniotes such as tilapia and cuttlefish, this study has been the first to show evidence of such cryptic colour change triggered by dermal light perception in amniotes.

Elina Rantanen





New Journal of Zoology Podcast

30 04 2015

A new episode of the Journal of Zoology podcast is now available and you can listen to it here.

In this episode, we will hear from Pierre-Paul Bitton and Brendan Graham about the success of European starlings colonising North America and how this phenomenon may have been aided by their wing morphology, Madlen Ziege tells us how the burrow structure of European rabbits changes as they move from the countryside into cities, and we learn from Megan Owen how polar bears communicate via scent from their paws!

You may subscribe in iTunes to receive the latest Journal of Zoology podcasts.

Elina Rantanen





Recently Published in the Journal

16 03 2015

What animals can live in cryoconite holes? A faunal review

Zawierucha, M. Kolicka, N. Takeuchi and Ł. Kaczmarek

Glaciers support a whole range of life, from bacteria and algae to more complex organisms such as mosses, nematodes and arachnids, despite their harsh environmental conditions. Indeed, it has been suggested that glaciers should be treated as a new biome altogether. Cryoconite holes, which are small, water-filled reservoirs on the surface of glaciers, form microecosystems complete with simple trophic webs that sustain primary producers and primary and even secondary consumers. Cryoconite holes are formed when windblown dust or soot land on the surface of a glacier and start melting the ice, as they absorb heat from the sun owing to their dark colour. In their article published in the Journal of Zoology, Krzysztof Zawierucha and his co-authors provided the first comprehensive review of the fauna found living in cryoconite holes on glaciers around the globe. They found that only 26 papers published since 1885 have reported on cryoconite hole fauna, and these studies were conducted on glaciers located in the Arctic, Antarctic, Patagonia, Alps and Himalayas. These papers had found invertebrates from five phyla (Rotifera, Annelida, Tardigrada, Nematoda and Arthropoda) and 41 taxa living in cryoconite holes, forming basic food webs where primary consumers feeding on microbes and algae are prey to secondary consumers.

Raven Glacier; photo by Frank Kovalchek

Raven glacier, photo by Frank Kovalchek

Moreover, some of these animals are specifically adapted to these extreme environments: they may enter anabiosis in unfavourable conditions or produce dormant eggs, or have black pigment granules in their epidermis to protect them from the high levels of UV radiation, particularly in the polar regions. Furthermore, other studies have found in cryoconite holes bacteria that produce special antifreeze proteins. Further research will probably find more taxa inhabiting cryconite holes, and improve our understanding on how organisms adapt to living in these extreme environments. However, accelerated melting of glaciers due to climate change means that these ecosystems are disappearing at increasing rates, making them one of the most endangered ecosystems in the world.

Elina Rantanen





Author Spotlight: Adrian Barnett

4 02 2015

More food or fewer predators? The benefits to birds of associating with a Neotropical primate varies with their foraging strategy

A. Barnett and P. Shaw; Journal of Zoology, Vol. 294, Issue 4, pages 224–233, December 2014

Adrian Barnett

Adrian Barnett; photo by Eliana dos Santos

With some studies, you go into the field site with the idea and a series of questions ready formed, while others leap out and clamour for your attention while you are already there and doing something else. The study on uacaris and their influence on the foraging success of bird species is an example of the second.

With a group of Brazilian biologists, I was researching the feeding ecology of the Golden-backed uacari, a monkey which lives in igapó, the seasonally-flooded forests along the sides of blackwater rivers in central Amazonian Brazil. At the time almost nothing was known about the animal’s lifestyle, so what it ate seemed a pretty good place to start.

Paddling our small wooden canoes through the igapó we noticed that small antbirds would follow uacaris whenever they were in their territory. They would move along in the general direction of the uacari band, stopping when the monkeys left the bird’s territory. This didn’t make a lot of sense initially, because the antbirds feed on tiny insects that live in the moss and crevices on treetrunks. Not the kind of insects that you’d imagine get disturbed by a band of monkeys.

It was a different story, though, with the nunbirds and the jacamars, who are sit-and-wait predators feeding on grasshoppers and moths – exactly the kind of insects you can imagine leaping out of the way when monkeys are crashing around. Checking out how often these birds made their feeding sallies when monkeys were and were not around, we found that, indeed, yes, they fed more when monkeys were present. But what about the antbirds?

Golden-backed uacari; photo by Bruna M. Bezerra

Golden-backed uacari; photo by Bruna M. Bezerra

Well, it turns out that its not only grasshoppers that get out of the way of monkeys, small hawks do too. We’re not sure if its because they just find the monkeys annoying and leave, or if its because eagles feed on the monkeys and tend to follow them. And eagles also eat hawks. Either way, the upshot is that when and where there are monkeys there are fewer hawks. Which is good news for the antbirds, because its exactly these small hawks that are their major predators.

So, there is quite a lot going on, with two different groups of birds benefiting from the monkeys’ rumbuctious activities in quite different ways (while the hawks are probably off cursing in a corner somewhere).

Igapo forest in the Amazon; photo by Adrian Barnett

Igapo forest in the Amazon; photo by Adrian Barnett

Not only does it show the complexity of ecological interactions, the study is only the second time that anyone has actually shown that the presence of monkeys can increase feeding rates in some birds. People seeing monkeys and birds together have always assumed that the primates are acting as some sort of beater, but only one other study (on how gorillas visiting swamps increase lilly-trotter feeding rates) had actually shown it.

The work was done in Jau National Park in central Amazonian Brazil, and we continue our work there, trying to unravel the fascinating ecology of the seasonally-flooded igapó forests in which the monkeys and the birds in this study make their home.

Adrian Barnett

University of Roehampton / Instituto Nacional de Pesquisas da Amazônia





New Journal of Zoology Podcast

18 12 2014

A new episode of the Journal of Zoology podcast is now available and you can listen to it here.

Journal of Zoology podcastIn this episode, Tacyana Oliveira tells us about sound production and use in seahorses and other fish, we will learn from Philip Bateman how urban grey squirrels in New York react to humans and monitor their behaviour, and Anthony Herrel talks to us about behavioural syndromes and exploration behaviour in amphibians.

You may subscribe in iTunes to receive the latest Journal of Zoology podcasts.

Elina Rantanen





Recently Published in the Journal

17 10 2014
L. S. L. Hohl, M. F. C. Loguercio, R. A. Buendía, M. Almeida-Santos, L. A. Viana, J. D. Barros-Filho and O. Rocha-Barbosa

How does an animal with no limbs dig its way through compact soil? In this study recently published in Journal of Zoology, the authors used for the first time X-ray emission to film excavation behaviour and performance of amphisbaenids, burrowing legless reptiles that are able to dig permanent underground galleries in heavily compacted soils. Amphisbaenids have specific adaptations to fossorial locomotion: their skin is only loosely connected to their body so that the trunk can move backwards and forwards inside the skin, and their skulls are strongly ossified and compacted, and can be shaped like a shovel or a spade.

An amphisbaenid Leposternon microcephalum, photo by Leandro Hohl

An amphisbaenid Leposternon microcephalum, photo by Leandro Hohl

As supplementary material to their paper, the authors provided a video (available here) of the forwards and backwards locomotion of an amphisbaenid within a substrate. Using videofluoroscopy, the authors were also able to describe for the first time the unique backwards movement of amphisbaenids in their tunnels. As can be seen on the video, during the backwards movement the vertebral column of the animal moves independently from the skin, forming ‘waves’ inside its body. This new technology will enable further investigations and analyses of the fossorial locomotion of these unique animals.

Elina Rantanen

Fluoroscopy Procedure, photo by Mariana Fiuza de Castro Loguercio

Fluoroscopy Procedure, photo by Mariana Fiuza de Castro Loguercio

X-ray image of an amphisbaenid, photo by Mariana Fiuza de Castro Loguercio

X-ray image of an amphisbaenid, photo by Mariana Fiuza de Castro Loguercio





Virtual Issue: Sound Production Mechanisms in Animals

1 09 2014

Elodie F. Briefer

Institute of Agricultural Sciences, ETH Zürich, Universitätstrasse 2, 8092 Zürich, Switzerland

Journal of Zoology Virtual IssueAcoustic communication is used by Arthropodes and Vertebrates, and particularly in species that move in the three-dimensional space (e.g. underwater or in forests), in order to communicate at both short and long distances. This mode of communication is highly developed in social species, and plays a crucial role in reproduction, parent-offspring communication, predator avoidance, territoriality, foraging and group communication. The modes of production of sounds and the structures used in sound production are very diverse and range from vibration of the wings in fruit flies (Drosophila) to stridulation in crickets, snapping of the swimbladder in fish, tongue clicks in some bats and vibration of the tympaniform membranes in birds or of the vocal cords in mammals. Several seminal papers on the modes of acoustic production and its link with the acoustic structure of vocalisations, as well as on the information content of vocalisations, have been published in Journal of Zoology. This free Virtual Issue gathers a selection of reviews and research papers, from various years, on the topic of sound production mechanisms in animals.

In the first selected paper, Parmentier et al. (2008) compared the structures involved in acoustic communication in three species of pearlfish (Carapidae; Carapus boraborensis, Encheliophis gracilis and Carapus homei). These small eel-like fish produce species-specific sounds that differ in temporal parameters, spectral frequencies, and sound intensity. In these species, sounds are produced through the swimbladder. The contraction of primary sonic muscles pulls the anterior bladder. When releasing the tension, the swimbladder snaps back to its resting position, producing sound. The authors analysed the sound production system as well as the acoustic features of the sounds produced. They were able to relate each part of the sounds to the action of swimbladder muscles. They also showed anatomical as well as acoustic differences between the three studied species.

With the second and third paper selected for this Virtual Issue, we move on to bird sound production. These two papers, by Thorpe (1958) and Warner (1972), are among the earliest detailed papers on the topic of sound production mechanism in birds. Thorpe (1958) is a review paper describing the vocal apparatus of birds and comparing it with human vocal apparatus. Both bird vocalisation and human voice are produced by the vibration of membranes during the exhalant phase of respiration (tympaniform membranes and vocal cords, respectively). This sound is then shaped in the resonance cavities (vocal tract above the syrinx and larynx, respectively). Warner (1972), after a historical review of previous work conducted on sound production mechanism in birds, compared the anatomy of the syrinx in several passerines birds (songbirds). His main finding is that the only demonstrable vibratile areas, hence the only sound sources, in the syrinx are the internal tympaniform membranes. These membranes, located one in each bronchus, can vibrate independently of each other, thus producing two harmonically unrelated tones at the same time (biphonation). These findings would be confirmed later on by many other studies.

Most bats produce echolocation signals, ranging from 20 to 200 kilohertz in frequency, using their larynx. However, some variation exists. For instance, a few species click their tongue, whereas horseshoe and leaf-nosed bats emit their echolocation calls through their nostrils, which are surrounded by a fleshy, horseshoe/leaf-like structure. In the fourth paper of this Virtual Issue, Robinson (1996) investigated the function of the noseleaf of horseshoe and leaf-nosed bats in echolocation. The author measured the echolocation frequency, noseleaf width, and forearm length of 14 species from the genera Rhinolophus and Hipposideros. This study revealed that noseleaf width is related to the wavelength of the echolocation signal, but not to forearm length. This suggests that noseleaf width is determined by wavelength rather than body size, thus highlighting the function of noseleaf in the production of echolocation signals.

The next paper selected for this Virtual Issue, by Sissom et al. (1991), investigates purring in cats. The mechanisms of cat purring have turned out to be challenging to understand. Indeed, the very low fundamental frequency of purring, notably in domestic cats (around 25 Hertz), suggests alternative mechanisms of sound production than flow-induced vocal cord vibration, as only very long cords could produce such low frequency. Proposed mechanisms include aerodynamic and hemodynamic vibration of the true and false vocal chords, the soft palate, and the arterial system, or muscular vibrations of the diaphragm and a repetitive closing of the glottis. The authors recorded domestic cats in a shelter and found that purring occurs during the entire respiratory cycle, with a fundamental frequency ranging between 23 and 31 Hertz. This frequency is higher during expiration than inspiration, but is quite stable throughout the life of an individual, and is not related to its weight or sex. Their results support the laryngeal mechanism but argue against the mechanical involvement of the diaphragm and intercostal muscles. Thus, purring could arise from the gating of respiratory flow by the larynx. This had been suggested also by Remmers and Gautier (1972), who showed that purring is in fact produced by active contractions of laryngeal muscles modulating the respiratory air flow passing through the vocal cords, as opposed to flow-induced self-sustaining oscillations found, for example, in humans.

According to the source-filter theory of voice production (Fant, 1960; Titze, 1994), the air flow coming from the lungs induces the oscillation of the vocal cords, thus producing the “source” sound. This sound is then filtered in the vocal tract (“filter”). Some frequencies, which correspond to the resonances of the vocal tract, will be amplified and other frequencies will be dampened. The source determines the lowest frequency of the voice (fundamental frequency) and its harmonics, while the filter determines the spectral peaks, called “formants”. In human voice, the pattern of the first two formants allows to distinguish between different vowels and is thus the basis of human speech. The source-filter theory framework has been recently adapted to other animals. The sixth paper of this Virtual Issue, by Taylor and Reby (2010), describes how mammal communication research benefited from this framework. By linking the structure of vocalizations to their mode of production, researchers have been able to highlight information, in vocalisations, about the sender’s body size, age, sex, hormonal levels, dominance status and even motivational or emotional state. This review paper describes the source-filter theory in details and the indices that are generated at the source and at the filter. The seventh paper of the Virtual Issue, by Briefer (2012), describes in more details how motivational or emotional states can affect vocalisations in humans and other mammals. In this paper, I reviewed the existing literature on vocal correlates of emotions in several mammals, in order to highlight common patterns of changes in vocal parameters and find the best source- and filter-related parameters that can reliably indicate the two main dimensions of emotions (arousal and valence).

The eighth paper selected for this Virtual Issue, by Fitch (1999), shows how the source-filter theory framework can be applied to birds, in order to explain the evolution of trachea elongation. More than 60 bird species possess an elongated trachea. Formant frequencies depend on the vocal tract length and shape, with lower frequencies indicating longer vocal tracts. Normally, the vocal tract is constrained by surrounding bones, so that its length strongly depends on body size. Formants are thus good indicators of body size in many species. However, some species possess either a mobile larynx that they can retract to lengthen the vocal tract during vocalisations (e.g. red deer and fallow deer), or possess an elongated vocal tract. Fitch suggests that these characteristics evolved through sexual selection to exaggerate perceived body size, as animals can produce vocalisations with lower formants than expected from their body size.

The ninth paper selected for this Virtual Issue investigated the source of vocal production in muskoxen (Ovibos moschatus), a large ungulate of the family Bovidae and subfamily Caprinae. Although highly sexually dimorphic (males are 1/3 heavier than females), both sexes of this species produce very low roars. In this paper, Frey et al. (2005) investigated the laryngeal anatomy and the roaring vocalizations of the muskox. Roars in both sexes are characterised by a pulsed structure, with a pulse rate of 20 Hz on average. The larynx size of adult male and female are remarkably similar (i.e. almost identical larynx size and vocal cord length). Both sexes possess a potentially inflatable ventrorostral laryngeal ventricle, which could serve to increase the amplitude of roaring or to act as an additional resonance space. The only difference between the sexes is a voluminous fat pad in the medial portions of the vocal cords of adult males, but not of females. However, this pad does not seem to induce important differences between the pitch of males and females. Muskoxen thus differ from other species with similar mating systems (e.g. fallow deer, red deer, elephant seals), in which strong sexual dimorphism is accompanied by distinct acoustic differences.

The two last papers selected for this Virtual Issue on sound production mechanism investigated the link between vocal tract length and formant frequencies in canids (Plotsky et al. 2013) and fallow deer (McElligott et al. 2006), respectively. Plotsky et al. (2013) present one of the first clear evidence that formants provide good, honest vocal cues of signaller size. The authors tested the link between vocal tract length, measured from X-ray images, and measures of body size in Portuguese water dogs (Canis lupus familiaris) and Russian silver foxes (Vulpes vulpes). They show that the oral component of the vocal tract, which determines formant frequencies, is strongly related to body size. McElligott et al. (2006) investigated the link between vocal tract elongation and formant frequencies in fallow deer (Dama dama). This species possesses a mobile larynx that can be retracted during vocalizations. The authors show, using audio and video recordings of mature, groaning fallow bucks, that individuals can increase their vocal tract length on average by 52% during vocalization. The highest formants (3-6), which strongly depend on the vocal tract length, are lowered, while the lowest formants (1-2), which depend more on the shape of the vocal tract, show minimal change during laryngeal retraction. This phenomenon could be used by males to exaggerate their perceived body size.

We hope that you enjoy reading this free collection of papers on various modes of sound production and adaptions published in Journal of Zoology.

 

References

Fant, G. (1960). Acoustic theory of speech production. The Hague: Mouton.

Remmers, J.E. and H. Gautier, Neural and Mechanical Mechanisms of Feline Purring. Respiration Physiology, 1972. 16: p. 351-361.

Titze, I.R. (1994). Principles of vocal production. Englewood Cliffs: Prentice-Hall.








Follow

Get every new post delivered to your Inbox.

Join 91 other followers