The astonishing diversity of great tit song

As I was coming home from work yesterday there was an unmistakable feeling of spring in the air. After what feels like a very long and harsh winter (it dropped to an incredible -16°c for a few days) the sunshine and warmth is certainly welcome.

It’s not just me that’s enjoying the sunshine either. At this time of year the breeding season for great tits (Parus major) really gets going and when the sun shines the males sing as they attempt to attract females to their territories.

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Great tits sing from around February to early June

For some people the first snowdrops mark the start of spring, for others the melting snow or the lengthening days. For me, great tit song signals that spring is on its way and is always a welcome sound.

Great tit song is one of the most distinctive sounds in nature. From February until early June these little birds can be heard singing in fields, parks, woodlands and even in the middle of cities from Ireland all the way to China.

The most common great tit song contains two repeating notes, one high and one low which are said to sound a bit like “tea-cher, tea-tea-cher”. Here is an example I recorded in Derby (UK) a few years ago with a spectrogram below so you can see how it looks.

great-tit-spectrogram-derbyRemarkably however, this is just one of over 70 different calls and songs great tits are known to produce with individual birds having repertoires of up to eight song types. In fact, the great tit’s musical repertoire is so vast that if you hear a bird song you don’t recognise there is a good chance it’s a great tit!

Here a few different variants on the “classic” great tit call I have recorded in the past with spectrograms so you can see the difference.

Recorded in Starnberg (Germany)

great-tit-spectrogram-starnberg

Recorded in Bath (UK)

great-tit-spectrogram-bath

Recorded in Durham (UK)

great-tit-spectrogram-durham

Recorded in Leamington Spa (UK)

great-tit-spectrogram-leamington

In the past I travelled all over the UK recording these birds as part of my research. I have recorded so many great tit songs that I have an almost Pavlovian response whenever I hear one as I feel the need to grab my microphone and start recording. This year however, all I need to do when I hear their song is look forward to longer days and better weather.

Urbanisation is changing the way birds sing

ResearchBlogging.orgIn 1800 only 3% of the world’s population lived in urban areas, yet as the industrial revolution picked up pace in the early 18th and 19th centuries the number of people moving from the countryside to work in the newly industrialised cities soared. By 1950 29% of the world’s population were living in cities and by 1985 this had grown to 42% while in 2025 it is estimated to that it will be over 60%1. That is just 10 years from now. In highly developed nations such as those in Western Europe and North America the 50% threshold has already been surpassed which means that if you live in a western nation and do not live in a city you are in a minority.

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Across the globe cities are expanding.

It’s not just where people choose to live that is rapidly changing either, but how many of us there are. The human population is currently expanding more rapidly than ever before and has grown from just a few hundred million people less than a thousand years ago to over 7 billion today, and this number is still rising2. As the human population grows cities are expanding quickly to meet the need for additional housing while the surrounding countryside is farmed and developed ever more intensely to provide us with the food, water and other resources we need to live.

Human population growth from around 5 million people in 8000 BCE to over 7 billion today. (figure from Keinen and Clark 2012).
Human population growth from around 5 million people in 8000 BCE to over 7 billion today. (figure from Keinen and Clark 2012).

Naturally, many people are concerned about how we are going to continue to feed and clothe ourselves as populations continue to expand, but there is also a growing concern among many about how such huge numbers of people are affecting the environment and the animals that inhabit it.

For animals which depend on natural habitats such as forests, meadows, or wetlands to survive, the growth of urban areas often spells bad news as these habitats are removed and paved over to make way for new suburbs, factories and roads. In the UK numerous species have declined for just this reason. For example, the bittern, a close relative of herons, was once widespread in reedbeds and wetlands across the UK but is now confined to a tiny area of the south-east after its habitats were drained to make way for agriculture and urban developments.

While many species cannot survive in urbanised areas, others are able to tolerate moderate levels of urbanisation and may continue living within cities despite drastic changes to their habitats. Life in the city is not without its challenges however, even for the most adaptable and resilient of species. Cities typically contain different threats to rural areas such as an abundance of cats which are responsible for killing huge numbers of birds and small mammals4, and high levels of chemical5, light6 and noise pollution7 which all have negative impacts.

This all sounds bad, and it really is, but while many species suffer badly from the effects of increasing urbanisation and habitat loss, there are a few species that have been able to adjust remarkably well to life in urban areas. One group that has been particularly well-studied in this regard are the songbirds and over the past 15 years or so, biologists have discovered some fascinating behavioural adaptations which have allowed some species to become successful city dwellers.

Great tits are one species which are adapting to city life,
Great tits are one species which are adapting to city life.

One of the most notable features of cities across the world is that they are incredibly noisy places. With heavy traffic, building sites, aircraft flying overhead and all manner of other sounds and distractions it’s a miracle anyone can hear anything at all. For songbirds however, all this noise is more than just a distraction, it can seriously affect their chances of finding mates and successfully reproducing and for males it is likely to affect how well they can defend their territories against rivals.

While we may find bird song pleasant to listen to (or annoying depending on how early in the morning it is), for songbirds it has a serious purpose. Males sing during the breeding season to attract females8 and to signal to other males that their territory is occupied and should not be entered9.

City noise can overlap and interfere with these signals making communication among birds difficult and unreliable. The background noise of a city is typically continuous low rumble concentrated at around 2kHz in frequency. Unfortunately for many birds this overlaps neatly with the frequency of their songs and this can make it difficult for other birds to hear them as they do not stand out from the irrelevant background noise.

Clearly this is a problem for birds which rely on song to communicate, yet research has revealed that birds have ways of overcoming this problem and one of them is to increase the frequency at which they sing so that their songs literally rise above the background noise and can be clearly heard.

Great tits sing at a higher frequency in noisy cities than in quieter rural areas (from Mockford and Marshall, 2009).
Sonograms of rural (a) and urban (c) great tit song compared to the background noise of a city (b). You can clearly see that the urban song is a higher frequency than rural song and above the frequency of the city noise. (from Mockford and Marshall, 2009).

Evidence that birds sing at higher frequencies in noisy cities than they do in quieter rural sites has now been found in numerous species including great tits (Parus major)7, blackbirds (Turdus merula)10, European robins (Erithacus rubecula)11 and song sparrows (Melospiza melodia)12.

In great tits the difference in song frequency between urban and rural sites has been measured at 478Hz13 and tests have shown that this is enough to substantially improve the distance over which song can travel in urban environments before it degrades and becomes inaudible14.

Birds may also face challenging noisy conditions in natural environments too such as where running water or wind creates high levels of low-frequency noise and these naturally noisy sites have allowed scientists to confirm that it really is the noise in cities and not some other factor which is causing city birds to sing at high frequencies. Biologists Henrik Brumm and Hans Slabbekoorn recorded the songs of white-throated dippers (Cinclus cinclus) living around noisy fast flowing streams in Scotland and found that they call at frequencies well above that of the background noise and higher than usual for this species suggesting that dippers in this area have adapted their calls to suit their noisy habitat15.

dipper
Dippers close to noisy streams sing at a higher frequency than the background noise so their songs can be heard (from Brumm and Slabbekoorn, 2005).

The effect of natural background noise on song frequency has also been shown in African little greenbuls (Andropadus virens) which sing at a higher frequency in areas where the rainforest is merging with open grasslands (known as ecotone forests) than they do deep within the rainforest itself16. Analysis of these two habitats revealed that the background noise in the rainforest is largely concentrated at higher frequencies while in ecotone forests there is more low-frequency noise. By singing at a lower frequency little greenbuls within the rainforest can ensure that their song does not overlap with the higher frequency background noise found in rainforests, while by singing at a lower frequency little greenbuls in ecotone forests avoid the lower frequency background noise in their habitat.

The evidence that birds change the frequency of their songs as an adaptation to noisy conditions may seem quite conclusive but not everyone agrees. An alternative explanation for the observed frequency shifts is that higher frequency song is actually just an unavoidable and possibly unimportant side-effect of singing more loudly, and it is higher volume, not frequency, which allows birds in noisy environments to overcome the background noise17.

In support of this argument Erwin Nemeth and Henrik Brumm of the Max Planck Institute for Ornithology in Germany found that the typical increases in song frequency found in great tits and blackbirds may be too low to substantially improve signal transmission whereas small increases in song amplitude were found to increase the distance over which a bird’s song could be detected much more effectively18.

But why should song frequency increase when birds sing more loudly? Nemeth and Brumm suggest two possibilities. Firstly, the increase in frequency observed in songs in noisy environments could be a side-effect of what is known as the Lombard effect (named after the French scientist Étienne Lombard) in which animals unconsciously increase the volume and frequency of their calls when the level of the background noise rises.

Nachtigall_%28Luscinia_megarhynchos%29-2[1]
Nightingales in Berlin sing loudly to ensure that they are heard.

The Lombard effect is known to occur in humans (this is why it might feel like you have to shout to be heard at loud parties) and has also been shown in both lab and field studies of songbirds. Lab experiments on elegant crested tinamous (Eudromia elegans)19, and budgerigars (Melopsittacus undulates)20, have shown that these species both sing more loudly and at a higher frequency when background noise increases and the same result has been shown in the field in a study of Nightingales (Luscinia megarhynchos) in Berlin21.

A second reason why song frequency may increase when birds sing more loudly is that both the volume and frequency of bird songs depend on the same song producing organ which could limit how well birds can independently control frequency and volume. In birds this organ is the syrinx which is the bird equivalent of the mammalian larynx or voice box and is located at the base of the windpipe connected to the lungs. Birds produce song by forcing air at high pressure from the lungs through the syrinx causing membranes to vibrate creating sound. This sound can then be modified using numerous tiny muscles which alter the shape and tension of the sound producing membranes.

However, past studies of the avian vocal system have shown that without these tiny muscles altering the structure of the sound, both the frequency and amplitude of bird song unavoidably increase together. In other words, when birds sing louder they cannot help but also sing at a higher frequency22.

Of course, this may be totally irrelevant if birds are able to use muscles to independently control the frequency and volume of their songs but there is evidence to suggest that the frequency and volume of bird songs really are closely intertwined. One of the clearest examples of this comes from a study by Nemeth and his colleagues at the Max Planck institute who recorded blackbirds singing in sound-proof chambers and showed that volume and frequency really were strongly correlated17. When blackbirds sing more loudly they also sing at a higher frequency and this may be totally involuntary. Similar results have been found in other species including zebra finches (Taeniopygia guttata)23 and song doves (Streptopelia risoria)24 suggesting that this pattern may be widespread in birds as a whole.

1280px-Turdus_merula_-Gran_Canaria%2C_Canary_Islands%2C_Spain-8_%282%29[1]
When blackbirds increase the volume of the song they also sing at a higher frequency. (image credit Juan Emilio).

It has become very clear over the past few years that urban noise is causing bird song to change however, opinion is still divided on whether it is the frequency or amplitude changes that are most important to improving song transmission in noisy environments. It is possible that both have important roles to play in helping birds to adapt to noisy urban areas and hopefully future research will provide an answer to this question.

The study of how urban noise affects bird song is a very active area of research and there are many unresolved questions which are likely to be answered in the next few years. Most importantly we need to find out what the long-term impacts of urban noise are on bird populations. Although many species of birds do seem to be able to adapt to noise we do not know how the dramatic changes we are causing to their environments will affect them in the long-term. Furthermore, many species are not able to adapt to urban areas for numerous possible reasons. They may not possess the behavioural flexibility to cope with new environments or not they might not be physiologically capable of changes their songs or behaviour. That is why studies those discussed here matter, we are changing the planet in ways which have never been seen before and we know that many species are suffering as a result. The first step to protecting animals from these changes is to understand how they are affected and that is just what these studies aim to do.


References

1. Kegel, B (2014).Tiere in der Stadt: Eine Naturgeschichte. Köln: DuMont Buchverlag. (In German).

2. Keinan, A., & Clark, A. (2012). Recent Explosive Human Population Growth Has Resulted in an Excess of Rare Genetic Variants. Science, 336 (6082), 740-743 DOI: 10.1126/science.1217283

3. Barnosky AD, Matzke N, Tomiya S, Wogan GO, Swartz B, Quental TB, Marshall C, McGuire JL, Lindsey EL, Maguire KC, Mersey B, & Ferrer EA (2011). Has the Earth’s sixth mass extinction already arrived?. Nature, 471 (7336), 51-7 PMID: 21368823

4. van Heezik, Y., Smyth, A., Adams, A., & Gordon, J. (2010). Do domestic cats impose an unsustainable harvest on urban bird populations?. Biological Conservation, 143 (1), 121-130 DOI: 10.1016/j.biocon.2009.09.013

5. Liker A, Papp Z, Bókony V, & Lendvai AZ (2008). Lean birds in the city: body size and condition of house sparrows along the urbanization gradient. The Journal of animal ecology, 77 (4), 789-95 PMID: 18479344

6. Miller, M. (2006). Apparent Effects of Light Pollution on Singing Behavior of American Robins. The Condor, 108 (1) DOI: 10.1650/0010-5422(2006)108[0130:AEOLPO]2.0.CO;2

7. Slabbekoorn, H., & Peet, M. (2003). Ecology: Birds sing at a higher pitch in urban noise. Nature, 424 (6946), 267-267 DOI: 10.1038/424267a

8. Baker, M., Bjerke, T., Lampe, H., & Espmark, Y. (1986). Sexual Response of Female Great Tits to Variation in Size of Males’ Song Repertoires. The American Naturalist, 128 (4) DOI: 10.1086/284582

9. Krebs, J., Ashcroft, R., & Webber, M. (1978). Song repertoires and territory defence in the great tit. Nature, 271 (5645), 539-542 DOI: 10.1038/271539a0

10. Nemeth, E., & Brumm, H. (2009). Blackbirds sing higher-pitched songs in cities: adaptation to habitat acoustics or side-effect of urbanization? Animal Behaviour, 78 (3), 637-641 DOI: 10.1016/j.anbehav.2009.06.016

11. McLaughlin, K., & Kunc, H. (2012). Experimentally increased noise levels change spatial and singing behaviour. Biology Letters DOI: 10.1098/rsbl.2012.0771

12. Wood, W., & Yezerinac, S. (2006). Song sparrow (Melospiza melodia) song varies with urban noise. The Auk, 123 (3) DOI: 10.1642/0004-8038(2006)123[650:SSMMSV]2.0.CO;2

13. Mockford, E., & Marshall, R. (2009). Effects of urban noise on song and response behaviour in great tits. Proceedings of the Royal Society B: Biological Sciences, 276 (1669), 2979-2985 DOI: 10.1098/rspb.2009.0586

14. Mockford, E., Marshall, R., & Dabelsteen, T. (2011). Degradation of Rural and Urban Great Tit Song: Testing Transmission Efficiency. PLoS ONE, 6 (12) DOI: 10.1371/journal.pone.0028242

15. Brumm, H., & Slabbekoorn, H. (2005). Acoustic communication in noise. Advances in the Study of Behavior, 35, 151-209 DOI: 10.1016/S0065-3454(05)35004-2

16. Slabbekoorn H, & Smith TB (2002). Habitat-dependent song divergence in the little greenbul: an analysis of environmental selection pressures on acoustic signals. Evolution; international journal of organic evolution, 56 (9), 1849-58 PMID: 12389730

17. Nemeth, E., Pieretti, N., Zollinger, S., Geberzahn, N., Partecke, J., Miranda, A., & Brumm, H. (2013). Bird song and anthropogenic noise: vocal constraints may explain why birds sing higher-frequency songs in cities. Proceedings of the Royal Society B: Biological Sciences, 280 (1754), 20122798-20122798 DOI: 10.1098/rspb.2012.2798

18. Nemeth, E., & Brumm, H. (2010). Birds and Anthropogenic Noise: Are Urban Songs Adaptive?. The American Naturalist, 176 (4), 465-475 DOI: 10.1086/656275

19. Schuster, S., Zollinger, S., Lesku, J., & Brumm, H. (2012). On the evolution of noise-dependent vocal plasticity in birds. Biology Letters, 8 (6), 913-916 DOI: 10.1098/rsbl.2012.0676

20. Osmanski, M., & Dooling, R. (2009). The effect of altered auditory feedback on control of vocal production in budgerigars (Melopsittacus undulatus). The Journal of the Acoustical Society of America, 126 (2) DOI: 10.1121/1.3158928

21. Brumm, H. (2004). The impact of environmental noise on song amplitude in a territorial bird. Journal of Animal Ecology, 73 (3), 434-440 DOI: 10.1111/j.0021-8790.2004.00814.x

22. Titze, I. R. (1994). Principles of voice production (pp. 279-306). Englewood Cliffs: Prentice Hall.

23. Cynx J, Lewis R, Tavel B, & Tse H (1998). Amplitude regulation of vocalizations in noise by a songbird, Taeniopygia guttata. Animal behaviour, 56 (1), 107-13 PMID: 9710467

24. Elemans, C., Zaccarelli, R., & Herzel, H. (2008). Biomechanics and control of vocalization in a non-songbird Journal of The Royal Society Interface, 5 (24), 691-703 DOI: 10.1098/rsif.2007.1237

Can we use anthropomorphic language in animal behaviour research?

A few months ago during the coffee break at an animal behaviour conference I was talking to a colleague about her research when she told me that to suggest that animals could feel fear or be afraid was anthropomorphism, the mistake of assigning of uniquely human characteristics to other animals. This view is not at all uncommon among practicing scientists and the term anthropomorphism is often extended to include a whole range of behavioural traits and emotions such as impatience, joy, expectation, boredom, anger, happiness or sadness, and yet there is good evidence that these emotions are not unique to humans. For example, dogs have been shown to exhibit jealousy, elephants have empathy, and Capuchin monkeys get visibly angry when treated unfairly as this video shows.

The possibility than animals can think for themselves is also often questioned and yet we know that some animals such as chimps and dolphins have a sense of self. There are also examples of animal behaviours that surely require some degree intelligence and forward planning such as innovative tool use by chimps and deception by ravens.

Deep in thought. Do chimps think like we do?
Deep in thought. Do chimps think like we do?

One of the main arguments against using anthropomorphic language to describe animal behaviours is that there is no way to know how an animal is really feeling, we can only describe what it looks like it’s feeling but not what’s actually happening inside it’s head. But the same is also true of humans, yet no one would question the use of anthropomorphic language to describe human behaviours.

If a person says they are excited we don’t actually know that what they feel as excitement is the same as what you or I feel as excitement, to them it may be a very different thing. All we can do is observe how that person acts and behaves and decide for ourselves if that matches up with our interpretation of what excitement is. The same is true of any emotion. If I say I am or happy or bored how could you tell that what I feel as happiness or boredom is the same as what you or anyone else feels as those things? At some point we have to use our subjective judgement to decide how a person is feeling. Do their actions match our expectations for a happy person? Then we can say they are happy. Do they behave as if they are sad? Then we can say they are sad. If this applies to humans then surely it can also apply to animals, at least in some cases.

I am not suggesting that we should abandon all caution and start using anthropomorphic terms carelessly. What I am suggesting is that so long as we clearly define our terms we should be able to use words like ‘afraid’ or ‘excited’ to describe animal behaviours when those terms well match what we see. If I want to describe anger in animals I should be able to use the word anger so long as I clearly state what I mean by the term and the behaviour that I am describing well matches what most of us would recognise as anger.

Of course, there are cases where using anthropomorphic terms really isn’t appropriate. If I read a paper that described ‘angry’ aphids or ‘jealous’ earthworms I would be dubious that those animals really could feel those emotions. In other cases I would have much less of a problem. Can chimps get angry? I think so. Are rats afraid of predators? It seems likely.

For many scientists, including people who I work with, the fear of using anthropomorphic language seems deeply ingrained and I think this affects how we view the behaviour of animals. Not all animals are mindless automatons that blindly follow their pre-programmed instincts. Many animals, especially among the vertebrates, have complex behaviours and emotions which are best described using the same terms we use for those things in human animals. I think it is time we started describing animals behaviours exactly as we see them. We must define our terms and we must be clear but so long as we are there should be little problem to this approach.

For those that still doubt that animals have can have thoughts and emotions like ours I recommend this TED talk.

For another view I also strongly recommend this post by Jilly at her blog fluffysciences

What do you think? If you have an opinion please leave a comment below.

 

 

Cooperative sperm, killer sperm and the competition for reproductive success

ResearchBlogging.org

In the closing paragraph of on the origin of species Darwin famously said that nature was a war in which individuals struggle against each other and the environment for survival. However, while survival may be important from an individuals point of view, from an evolutionary perspective mere survival is not enough. Reproduction is what matters and success or failure at producing offspring is what determines an individual’s evolutionary success. Of course, survival is important too, but only when it leads to reproduction.

In most species the reproductive success of females is limited by the rate at which they can produce offspring. When a female is pregnant or carrying eggs she has no choice but to wait until she has given birth or laid her eggs before she can reproduce again, and this can take a long time. Males have no such constraints to their reproductive success and can potentially mate with hundreds of females over their lifetime and raise an enormous number of offspring. The only thing stopping them is that there just aren’t enough females to go around. This shortage of females coupled with the need to reproduce leads to intense, and often aggressive, competition among males for limited mating opportunities.

Male red deer (Cervus elephus) compete for females by fighting
Male red deer (Cervus elephus) compete for mating opportunities by fighting

Male red deer (Cervus elephus) fight for their chance to mate by using their huge antlers to batter their rivals into submission, while male northern elephant seals (Mirounga angustirostris) grow to enormous sizes allowing them to dominate harems of many females and guard them against the advances of smaller, weaker males. Not all species are so aggressive in their tactics. Males of many bird species such as peacocks (Pavo cristatus) and birds of paradise produce fantastic and colourful displays with which they attempt to attract females, as do a large number of insects and fish. In these species, rather than fighting with each other, males try to out-perform and out-class each other in the hope that females will choose them while their rivals are left unwanted on the sidelines. This may seem a more peaceful strategy but make no mistake, although these males don’t actively fight each other the competition between them is every bit as intense as among more aggressive species.

Male peacock (Parvus cristatus) aim to attract females by out-perform their rivals displays.
Male peacock (Pavo cristatus) aim to attract females by out-performing the displays of rival males.

So fighting or displaying are two ways in which males can improve their reproductive chances, but what happens in species in which each female mates with lots of different males in quick succession? How is a male to improve his odds of being the true genetic father of the offspring? Well, as is often the case evolution has found a way and that way is called sperm competition (yes, really).

In species in which females mate promiscuously males compete not just for mating opportunities but also for direct access to eggs. In these cases competition between males happens after mating has occurred as the sperm of multiple males compete with each other within the females reproductive tract as they race towards the eggs. In species in which sperm competition is known to exist an incredible variety of different sperm adaptations have been found, all of which serve to improve the sperms chances of reaching the eggs first.

For individuals of many species adaptation to sperm competition simply means producing more sperm so as to swamp the sperm of their rivals and increase the odds that some of their sperm will make it to the eggs before anyone elses. For other species adaptation to sperm competition is more complex. For example, the wood mouse, Apodemus sylvaticus, has evolved sperm that have a hook-like structure on the head which allows them to intertwine with one another to form long sperm ‘trains’ which are much faster at swimming than individual sperm.

The sperm of the wood mouse (Apodemus sylvaticus). (a) Image of the sperm head with the hook clearly visible. (b) 50 sperm hooked together. (c) A clip from video footage of the sperm train. (d) Another view of the sperm train with an arrow and asterisk marking the position of hooks. (e) One sperm latching onto another. (f) Another view of a sperm hook.
The sperm of the wood mouse (Apodemus sylvaticus). (a) Image of the sperm head with the hook clearly visible. (b) 50 sperm hooked together. (c) A clip from video footage of the sperm train. (d) Another view of the sperm train with an arrow and asterisk marking the position of hooks. (e) One sperm latching onto another. (f) Another view of a sperm hook. Image from Moore et al. (2002).

In a similar and recently discovered case, a team led by Morgan Pearcy of the Université libre de Bruxelles looked for evidence of sperm competition in the desert ant, Cataglyphis savignyiThe queen ants of this species mate with up to 14 males in rapid succession and store their sperm jointly in a special storage organ called the spermatheca. Only those sperm which make it to this storage organ have any chance of fertilising an egg and so competition for access to the spermatheca is intense. In response to this pressure C. savignyi males have evolved highly cooperative sperm that team up into bundles of 50-100 cells which can swim much faster than they could alone and so are better able to outcompete their rivals.

Sperm from the desert ant Cataglyphis savignyi work together to increase their swimming speed. Image from Pearcy et al, (2014).
Sperm from the desert ant Cataglyphis savignyi work together to increase their swimming speed. Image from Pearcy et al, (2014).

It is not just the way sperm behave that can change due to sperm competition, the shape and function of sperm can change too. For example, Philip Byrne and his colleagues from the University of Western Australia found that in a group of Australian frogs those species under the most intense sperm competition produced sperm with the longest tails, possibly to improve their swimming speed. Other species known to have oddly shaped sperm include the water beetle Dytiscus marginalis which has sperm that fuse at the head into pairs with two tails, and the tiny fruit fly Drosophila bifurca which at 6cm long produces the longest sperm on earth.

Some species have taken a more sinister approach to sperm competition and have evolved infertile “parasperm” which contain enzymes capable of breaking down the sperm of rivals. A similar and fantastically named kamikaze sperm hypothesis has even been proposed for humans in which some sperm are adapted to kill the sperm of rivals rather than fertilise eggs. The evidence for this hypothesis is equivocal at best but given the adaptations that have been discovered in other species it is not entirely unbelievable. In fact, given the adaptations that have been discovered so far, almost nothing is completely unbelievable.


References

Sperm competition by producing large quantities of sperm
Moller, A. (1989). Ejaculate Quality, Testes Size and Sperm Production in Mammals Functional Ecology, 3 (1), 91-96 DOI: 10.2307/2389679

Sperm trains in the wood mouse
Moore H, Dvoráková K, Jenkins N, & Breed W (2002). Exceptional sperm cooperation in the wood mouse. Nature, 418 (6894), 174-7 PMID: 12110888

Cooperative sperm in the desert ant
Pearcy M, Delescaille N, Lybaert P, & Aron S (2014). Team swimming in ant spermatozoa. Biology letters, 10 (6) PMID: 24919705

Sperm competition in Australian frogs
Byrne PG, Simmons LW, & Roberts JD (2003). Sperm competition and the evolution of gamete morphology in frogs. Proceedings of the Royal Society B: Biological Sciences, 270 (1528), 2079-86 PMID: 14561298

The two tailed sperm of the water beetle
Mackie JB, & Walker MH (1974). A study of the conjugate sperm of the dytiscid water beetles Dytiscus marginalis and Colymbetes fuscus. Cell and tissue research, 148 (4), 505-19 PMID: 4836644

The world’s largest sperm in drosophila
Bjork A, Dallai R, & Pitnick S (2007). Adaptive modulation of sperm production rate in Drosophila bifurca, a species with giant sperm. Biology letters, 3 (5), 517-9 PMID: 17594959

Killer ‘parasperm’
Buckland-Nicks, J. (1998). Prosobranch parasperm: Sterile germ cells that promote paternity? Micron, 29 (4), 267-280 DOI: 10.1016/S0968-4328(97)00064-4

Kamikaze sperm
Baker, R., & Bellis, M. (1989). Elaboration of the Kamikaze Sperm Hypothesis: a reply to Harcourt Animal Behaviour, 37, 865-867 DOI: 10.1016/0003-3472(89)90074-2

Criticism of the kamikaze sperm hypothesis
Moore, H., Martin, M., & Birkhead, T. (1999). No evidence for killer sperm or other selective interactions between human spermatozoa in ejaculates of different males in vitro. Proceedings of the Royal Society B: Biological Sciences, 266 (1436), 2343-2350 DOI: 10.1098/rspb.1999.0929

A spider that masquerades as a bird dropping

ResearchBlogging.org
The power that natural selection has to sculpt both the appearance and the behaviours of creatures so that they intricately and precisely fit their respective environments is for me a source of endless fascination and wonder. Some of the most impressive examples of natural selection’s power lie among the mimics of the insect and spider world where a huge diversity of body forms are to be found, from insects which look uncannily like leaves or moss, to spiders that look just like ants. The benefits of these disguises vary from species to species. For many blending seamlessly into the background provides some protection against predators, while for others it allows them to creep up on their prey unnoticed or lure victims to their demise.

The south-east Asian orb-web spider known as Cyclosa ginnaga is a perfect example of how mimicry may be used to conceal an animal from its predators, in this case highly aggressive predatory wasps. Although by themselves individuals of this species are conspicuously silver in colour and not all that well disguised, they are able to spin white circular silk decorations which they stand on in the centre of their webs as a way of concealing themselves. That might not sound like a great way to hide but the size, shape and colour of the spider when viewed against the white background of its decoration look remarkably like a bird dropping which, of course, is of no interest to predators. This type of mimicry, in which animals mimic inanimate objects, is termed masquerading and the details of this particular case were recently published in a new paper by Min-Hui Liu and colleagues.

a) Cyclosa ginnaga standing on its web decoration. b) A bird dropping. Photos from Lui et al. (2014)
a) Cyclosa ginnaga standing on its web decoration.
b) A bird dropping.
Photos from Lui et al. (2014)

Liu and colleagues wanted to know if the decoration of C. ginnaga really did function as an anti-predator masquerade. To test this the researchers first used a technique called spectral reflectance imaging to examine how the spider and its decoration appears through the eyes of its predators. After all, what looks like a bird dropping to us may look completely different to a wasp. This method compared the way that light reflects from the body of the spider and its decoration to what is known about the sensitivity of insect eyes. The results were unequivocal, wasps cannot see the difference between bird droppings and the masquerade display of C. ginnaga.

bird dropping spider
A composite picture showing examples of Cyclosa ginnaga on its web on the second and fourth rows and bird droppings on the first and third rows. Image credit: Min-Hui Lui.

The crucial test however, was to show that mimicking a bird dropping really does reduce the predation risk for the spiders and lead to real fitness benefits for individuals. To do this the researchers divided 39 wild caught spiders into three groups. To one group they coloured the bodies of the spiders black while leaving their decorations untouched, to another they coloured the decorations black while leaving the spiders themselves untouched, and to the final group they coloured both the bodies of the spider and their decorations black. They then observed the frequency of predator attacks on each group over 13 days and compared this to the predation rate on untouched spiders. From these three groups a huge increase in predation was observed on those spiders that had only their decorations blackened. This suggests strongly that having a white decoration really does help C. ginnaga to hide itself from predators.

Figure from Lui et al. (2014) showing rates of predator attacks when the spider, the spiders decoration, or both were coloured black.
Figure from Lui et al. (2014) showing rates of predator attacks when the spider, the spiders decoration, or both were coloured black.

As shown in the figure above, when both the spider and its decoration were blackened no increase in the frequency of predator attacks was observed. This is not so surprising as in this case the black spider is likely to be well camouflaged against its black background. What is surprising  however, is that when the spiders body was blackened but the decoration was not there was also no increase in predator attacks. This seems strange since a black body on a white background might be expected to stand out very clearly to predators. It may be that the wasps recognise only silver spiders as their target species and so don’t see the black coloured spiders as potential prey. It could also be that when a black spider is on a white background it still looks like a bird dropping since bird droppings often have black bits in them. The authors don’t discuss this anomaly in their paper but it does cast doubt on the idea that the silver spider in combination with the white decoration together form a masquerade which reduces the risk of predation. Nonetheless it is clear from this study that the web decoration does substantially reduce predator attacks, why that is so remains an interesting question that is open for discussion.


Reference

Liu MH, Blamires SJ, Liao CP, & Tso IM (2014). Evidence of bird dropping masquerading by a spider to avoid predators. Scientific reports, 4 PMID: 24875182

Great tits hunt for Pipistrelle bats

ResearchBlogging.org
When under strong ecological pressure, or when a good opportunity arises, animals have often shown themselves to be surprisingly innovative in how they adapt to new pressures or take advantage of new resources. Many examples of this have been observed in the wild including the discovery of tool use by chimpanzees, problem solving in guppies and the development of a novel ‘body-slapping’ behaviour as a means of communication in grey seals. No behaviour has surprised me more however than the discovery that in Hungary a population of a small seed-eating song bird, the great tit (Parus major), has switched from its staple diet of seeds and insects and has learnt to search for, kill and eat hibernating bats (Pipistrellus pipistrellus).

At around five inches long great tits are small birds, but pipistrelle bats are even smaller at just an inch in size. During the winter these bats hibernate in cracks and crevices in dark caves or old buildings where they are safe and well hidden, but when they awaken they start making noises which draws the attention of nearby predators, including great tits.

A Great tit (Parus major). Not a typical carnivore.
A Great tit (Parus major). Not a typical carnivore.

The earliest suggestion that great tits might hunt for bats goes back to at least 1947 when a Swedish biologist named Olaf Ryberg observed dead bats in Sweden with “injury, caused e.g. by titmice (possibly also bigger birds)“. It was to be almost half a century before the subject was raised again when in 1996 a great tit was seen feeding on a dead bat in a cave in Poland. Three years later at the same site in Poland three more bats were found, one dead and two alive, with injuries which looked like they were caused by tit beaks. Despite these observations it was still not clear that in any of these cases great tits were actually hunting for bats actively and it remained a possibility that they were simply scavenging on bats which had already died. A chance observation of a great tit capturing a live pipistrelle in a cave in Hungary in 1996 provided the only evidence at this point that great tits ever actively preyed on live bats.

That first observation was made by Péter Estók from Germany’s Max Planck Institute for Ornithology and intrigued by what he had seen he and his research team returned to the cave in Hungary on three separate occasions from 2004 to 2009. Using experiments and old-fashioned observation  they aimed to discover whether feeding on bats by great tits was simply opportunistic, or whether great tits had learnt to deliberately and systematically hunt for and feed on pipistrelles.

A common pipistrelle bat (Pipistrellus pipistrellus). Image from http://www.naturephoto-cz.com/
A common pipistrelle bat (Pipistrellus pipistrellus). Image from http://www.naturephoto-cz.com/

The research team quickly found their answer. During the first winter of observations they witnessed great tits capture and consume live bats seventeen times in just ten days. Yet despite this it was still not known why this behaviour had developed in the first place.

One possibility was that great tits used bats as a last-ditch food source when their regular food was in short supply. To test this possibility the researchers left a mixture of sunflower seeds and bacon in feeders around the cave entrance to provide an easy and irresistible meal for any passing great tits. Sure enough, when plentiful food was provided they found that hunting for bats by great tits stopped almost completely with only one case observed over a ten-day period. This provided good evidence that feeding on bats was driven by an urgent need for food and did not represent a more general shift in diet.

Now just one question remained to be answered. How do great tits find the bats in the first place? It was thought that they might be able to home in on the bat’s calls so to test this possibility Estók recorded the bats and played their calls back to great tits from a speaker. Around 80% of the birds reacted strongly to the sounds often turning their heads towards the speaker and approaching to investigate. This was particularly interesting because in one study bat calls were shown to act as a deterrent to mammalian predators, possibly by signalling that the bats are awake and cannot be caught. For great tits however it seems that bat calls are far from a deterrent, possibly because they can easily outmanoeuvre a bat in flight.

Eight years passed between the first observation of a great tit preying on a live bat and the start of Estók’s study. Given that the typical lifespan of great tits is three years the birds observed in 2004 couldn’t possibly have been the same birds that were seen in 1996. This raises the fascinating possibility that the bat killing behaviour is passed from one generation to the next by some form of cultural transmission. Whether this is or is not the case is not yet known and so it seems there is still much to learn about the unassuming great tit.

                                                                            

References

For the study of great tits hunting bats

Estók P, Zsebok S, & Siemers BM (2010). Great tits search for, capture, kill and eat hibernating bats. Biology letters, 6 (1), 59-62 PMID: 19740892

Bat calls as a deterrent to mammalian predators

Martin, K., & Fenton, M. (1978). A possible defensive function for calls given by bats (Myotis lucifugus) arousing from torpor
Canadian Journal of Zoology, 56 (6), 1430-1432 DOI: 10.1139/z78-196

Innovative behaviour in other animals

Body slapping seals
Bishop, A., Lidstone-Scott, R., Pomeroy, P., & Twiss, S. (2013). Body slap: An innovative aggressive display by breeding male gray seals (Halichoerus grypusMarine Mammal Science DOI: 10.1111/mms.12059

Problem solving guppies
Laland KN, & Reader SM (1999). Foraging innovation in the guppy. Animal behaviour, 57 (2), 331-340 PMID: 10049472

Tool use in chimpanzees
Goodall, J. (1964). Tool-Using and Aimed Throwing in a Community of Free-Living Chimpanzees Nature, 201 (4926), 1264-1266 DOI: 10.1038/2011264a0

Awesome orcas

ResearchBlogging.org

It has been known for a long time that whales and dolphins are incredibly intelligent animals but it’s not often we see that intelligence so impressively displayed as when orcas (often called killer whales) hunt. Orcas can actually be divided into several different ‘types’ which are found in different areas of the world and often specialise in hunting different prey. Some, such as those around Norway and Greenland, are particularly adept at hunting herring and follow the fishes migration path. Others, such as those in the north-east Pacific are skilled salmon hunters, and some have even learnt to strip tuna fish from fisherman’s lines. There is one group however that outclasses them all, the orcas of the Antarctic peninsula have become specialised at taking seals from floating ice and the way they do it is simply breathtaking. Ingrid Visser and her colleagues were lucky enough to observe the attack in 2006 and described it like this

…one killer whale remained in position with its rostrum against the ice floe while four killer whales moved away from the ice floe with the seal on it. These four killer whales reappeared simultaneously, approximately 20 seconds later in line-abreast with all submerged just under the surface. All four were coordinated-swimming, with their left sides orientated towards the surface. A trail of bubbles emanated from each of the animals blowholes as they accelerated and passed directly under the ice floe, two on each side of the stationary killer whale. This generated a large wave, which tipped the ice floe initially towards the wave, then as the wave poured over and crested under the ice, it pivoted and tilted the ice in the other direction where the attacking whales were now waiting. The breaking wave washed the seal into the water…

Coordinated orcas about to launch a "wave washing" attack.
Coordinated orcas about to launch a “wave washing” attack.

This same hunting technique, sometimes termed “wave-washing”, was later filmed by the BBC for the series Frozen Planet (highly recommended if you haven’t yet seen it).

As someone who has worked with seals a lot over the last few years I have mixed feelings about this. On the one hand the seal is clearly distressed and is tormented for a very long time before it is finally killed, but on the other I can’t fail to be impressed by the skill and intelligence of the orcas that is required to pull off an attack like this. For this hunting strategy to be succesful there must be forward planning, and a high level of communication and coordination between individual orcas. These characteristics are not often associated with animals.

What is really interesting is that in the case described by Visser and her colleagues the seal was caught after around 15 minutes but then released and allowed back onto the ice. It then had to endure a second wave-washing attack before being finally killed almost 15 minutes later. Why did the orcas not kill and eat the seal immediately? The answer is not known, it could simply be play behaviour or, more interestingly, it may be that the adults are training their young to hunt. We clearly have a lot more to learn from these amazing animals and I expect there will be many more discoveries in the future.

                                                           

For a detailed description of this behaviour see:

Visser I.N., Smith T.G., Bullock I.D., Green G.D., Carlsson O.G.L. & Imberti S. (2008). Antarctic peninsula killer whales (Orcinus orca) hunt seals and a penguin on floating ice, Marine Mammal Science, 24 (1) 225-234. DOI: