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

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How does urbanization affect biodiversity?

Imagine that you’re standing in the very centre of a large city complete with roads, skyscrapers, traffic, noise and pollution. How much wildlife is there around you? How many species are there? How much of what you see is native?

Now imagine you walk in a straight line out of the city, for every mile you walk you stop and observe the wildlife, You count how many species there are (species richness) and how many individuals of each species there are (abundance). What you are measuring is biodiversity, the straight line you are walking along is a transect. By studying biodiversity at regular points along the transect you are able to observe changes as the habitat becomes increasingly rural, in turn this allows you to determine what effect (if any) the city has on biodiversity.

Approaching the city centre. Species rich or Species poor?

So, what might you expect to find? Does biodiversity increase or decrease in response to urbanization? Are different species found in cities than in rural areas? Is there no change at all?

Sadly, it is often the case that urbanization causes biodiversity to decline. As cities grow vital habitat is destroyed or fragmented into patches not big enough to support complex ecological communities. In the city, species may become endangered, or even locally extinct as previously natural areas are swallowed up by the urban jungle. In the United Kingdom for example, an increasing human population density, and the resulting increase in urban development were found to be the cause of 35% of scarce plant species extinctions in the counties surrounding urbanized areas (2). Similarly, in the United States urbanization has been found to be directly responsible for the endangerment of 275 species, only invasion by non-native species had a greater impact causing 305 species to become endangered (1). Ironically it is urban growth that is often responsible for the introduction of non-native species, either accidentally (e.g. the brown rat, Rattus norvegicus), or deliberately, for food, pets or for aesthetic reasons. Non-native plants for example, are often planted in urban and suburban gardens and subsequently “escape” into the wild (3).

Why does biodiversity decline in urban areas?

The growth of cities may cause biodiversity to decline by fragmenting or destroying large areas of natural habitat on which many species depend. The rising human population is driving the expansion of urban areas and increasing the demand for natural resources such as timber and fossil fuels. This inevitably leads to habitat destruction which has been called “the largest factor contributing to the current global extinction event”(4). The rate of urbanization is alarming, for example, in the city of Concepción, Chile, 1734ha of wetlands and 1417ha of agricultural land, forest and scrub was lost to urban development between 1975 and 2000 (5). Similarly, in the United States the amount of urbanized land has increased year on year since 1970. Over 5% of the US land surface is now urbanized, substantially exceeding the combined total of both conservancy and national park land cover (3).  Although there are many causes of habitat loss, urbanization has been shown to be one of the most damaging in terms of numbers of species lost or threatened (2).  Numerous studies have found that both the richness and abundance of native species including plants (1), mammals (6), insects (7) and amphibians (8) decrease in response to urbanization.

Closely related to habitat loss is habitat fragmentation which can be defined as the transformation of a large and continuous habitat into many smaller, isolated habitats. The expansion of cities causes the fragmentation of large areas of natural habitat through the construction of roads, houses and industry. In many cases all that remains are small remnant patches of the original habitat contained within the confines of the city. Biodiversity is greatly reduced when large areas of natural habitat are fragmented. Small habitat patches are unable to support the same level of genetic or taxanomic diversity as they formerly could (9), while some of the more sensitive species may become locally extinct (4).

How severely fragmentation affects biodiversity depends to a large extent on the size of habitat patch that remains. Many species require large contiguous habitat patches in order to maintain stable populations. Smaller patches therefore typically contain fewer species than do large patches. As an example, a study in the US looking at forest birds in fragmented and contiguous forests found that in fragmented forests brood parasitism and predation on the birds significantly increased whilst reproductive success declined (10). Similar effects have also been shown for reptiles. Predation pressure on the lizard Psammodromus algirus was found to increase as patch size decreased leading to the lizard’s  extinction in small patches while populations in large patches remained viable (11). Small patch size can also have genetic effects for example, it was found that populations of the plant Trillium camschatcense had much lower genetic diversity in fragmented habitat compared to those growing in contiguous habitat (12).

Understanding the impact of small patch size is critical for scientists and conservationists alike if biodiversity is to be preserved. However, it is not the only factor in need of consideration. The distance between habitat patches and the quality of the intervening land also have significant effects. For example, two closely spaced patches of woodland habitat separated by farmland are likely to be much more biodiverse than the same habitat isolated on either side of a city. Populations occupying habitat fragments are rarely self-sustaining, rather they act as sinks relying on immigration from larger stable populations to remain viable. As a result poor quality intervening habitat or a high degree of isolation may substantially reduce the long-term survival potential of fragment populations (12). Different species have different requirements, some may be able to tolerate high levels of fragmentation and isolation while other more sensitive species may not. However, if we are to preserve biodiversirty for the future reducing habitat loss and fragmentation should be priorities.

In addition to the twin effects of fragmentation and habitat loss there is another factor working to reduce biodiversity in urban areas. Biotic homogenization refers to the replacement of regional native (and often endemic) species with non-native, invasive and cosmopolitan species. Often it is the same non-native invasive species that are found in many cities worldwide (for example the rock dove Columba livia could be considered a global species), the result is a high species overlap between areas of formerly distinct biota, the homogenization of biological communities and a decrease in regional and global biodiversity (13, 14).

Many studies have shown that the expansion of the urban environment causes declines and local losses of native species including plants (1) and insects (15). As native species decline the number of non-native species rises. For example, as of 2006 New York city has lost 578 native species and gained 411 non-natives meanwhile, Massachusetts has lost over 330 native species and gained over 200 non-native species (16). It has been suggested that the increase of non-native species in urban areas may be due to one of two factors, (i) the importation into cities of non-native species and (ii) the city providing a favourable habitat for non-native species (16). Human settlements have been shown to provide ideal conditions for invasive and exotic species due to high levels of disturbance which tends to favour non-native species at the expense of native species (17).

The removal of native species from urban areas and their replacement with non-native species drastically alters the composition of urban biological communities, the ecology of cities is therefore very different to the surrounding undeveloped areas. For example urban bird communities are often composed of granivorous (seed eating) rather than insectivorous species (18), while insect communities have been shown to become more generalist towards the urban centre and more specialist in less urbanized environments (7).

Replacing native species with non-native species does not necessarily cause biotic homogenization. If different communities of non-native species replace native species at cities around the world then biotic differentiation rather than homogenization will have occurred. However, there is no evidence that this is happening. Many studies have shown that the extirpation of native species in urban environments and the influx and non-native invasive species is leading to global biotic homogenization. For example a study of urban bird populations from two distant locations (Ohio and California) found urban populations to be much more similar to each other than rural populations the same distance apart (19). Similarly, a study in Canada found that the ecology of cities across the country was becoming increasingly alike with many of the same species found in cities nationwide (14).

The trend towards global biotic homogenization of urban areas poses a serious threat to local, native species in countries around the world. The importation and introduction of exotic species is changing biological communities by forcing out local indigenous species, which may not be so well adapted to the urban environment, and replacing them with globally common and widespread species. If we are to preserve distinct regional species the importation of non-natives species should be discouraged and the diversity of native and indigenous species promoted and protected.

Does biodiversity always decline?

Perhaps surprisingly, no. Although many studies have found that declines in biodiversity and increasing urbanization are strongly correlated (5, 15), research has also shown that in some situations biodiversity actually peaks in suburban areas for certain groups such as insects (7), and plants (6). For example, it was found that in the Finnish city of Vantaa the number of vascular plant species was much higher on urban wasteland than in the surrounding forest. The reason being that wasteland contained large numbers of non-native introduced plant species while the forest did not (20).

Three explanations have been proposed that may explain the suburban peak in biodiversity, (i) The import of exotic species into urban areas increases species richness at a faster rate than native species are lost. (ii) Urban areas contain a large number of widely different habitats at small scales such as gardens, parks and wasteland. Each of these may provide very different habitats and so support a wide variety of species, urban gardens in particular are highly variable with no two containing quite the same combination of plants. (iii) The importation of large amounts of water, fertilizers and food into urban areas provides the nutrients required to significantly increase primary productivity. This in turn supports larger numbers of individuals than would be able to survive otherwise. These three proposals are not mutually exclusive, it is likely that all three (and possibly other factors) play a role in increasing urban biodiversity (6).

My research

I have been studying the effects of urbanization on biodiversity in the city of Leicester in the UK. By collecting arthropods along an urban-rural gradient I have been able to observe changes in species composition, richness and abundance. The diversity of arthropod communities then served as an indicator of the overall biodiversity of the sampling area.

Using sets of pitfall traps set at one mile intervals along the gradient, I collected just over 2000 arthropods belonging to more than 250 species over a period of one month. By identifying how many species and  individuals of each species were found at different locations along the gradient I was able to identify changes correlated with urbanization.

The aim of the study was to answer two questions. (i) Does urbanization affect biodiversity? And (ii) If so how?. Although these questions have been answered many times before the results have varied widely depending on location and experimental design of the studies. Previous studies have also often focused on a limited range of taxa such as bees (15) or plants (1), whereas this study aimed to examine biodiversity as a whole. Finally, with a few notable exceptions (1, 21) there has been little research of this type in Britain, the hope therefore, is that this study will provide an interesting insight into the response of Britain’s wild flora and fauna to urban development.

References

1. Thompson, K. and Jones, A. 1999. Human Population Density and Prediction of Local Plant Extinction in Britain. Conservation Biology. 13, 185-189.

2. Czech B, Krausman P.R, Devers P.K. 2000. Economic Associations Among Causes of Species Endangerment in the United States. BioScience 50, 593–601.

3. McKinney, M. 2002. Urbanization, Biodiversity and conservation. BioScience. 52, 883-890.

4. Fahrig, L. 2001. How Much Habitat is Enough?. Biological Conservation. 100, 65-74.

5. Paucharda, A., Aguayob, M., Peñaa, E., Urrutia, R. 2006. Multiple Effects of Urbanization on the Biodiversity of Developing Countries: The Case of a Fast-Growing Metropolitan Area (Concepción, Chile). Biological Conservation. 127, 272-281.

6. McKinney, M.L.. 2008. Effects of Urbanization on Species Richness – A Review of Plants and Animals. Urban Ecosystems. 11, 161-176.

7. McIntyre, N.E., Rangob, J., Faganb, W.F., Faeth, S.H. 2000. Ground Arthropod Community Structure in a Heterogeneous Urban Environment. Landscape and Urban Planning. 52, 257-274.

8. Riley, S.P.D., Busteed, G.T., Kats, L.B., Vandergon, T.L., Lee, L.F.S., Dagit, R.G., Kerby, J.L., Fisher, R.N., Sauvajot, R.M. 2005. Effects of Urbanization on the Distribution and Abundance of Amphibians and Invasive Species in Southern California Streams. Conservation Biology. 19 (6), 1894–1907.

9. Cane, J.H., Minckley, R.L., Kervin, L.J., Roulston, T.H., and Williams, N.M.. (2006). Complex Responses Within a Desert Bee Guild (Hymenoptera: Apiformes) to Urban Habitat Fragmentation. Ecological applications. 16 (2), 632–644.

10. Diaz, J.A., Carbonell R.,Virgos E., Santos T., Telleria J.L., 2000. Effects of forest fragmentation on the distribution of the lizard Psammodromus algirus. Animal Conservation. 3, 235–40.

11. Robinson, S.K., Thompson III, F.R., Donovan, T.M., Whitehead, D.R. and Faaborg, J.. (1995). Regional forest fragmentation and the nesting success of migratory birds. Science. 267 (5206), 1987-1990.

12. Tomimatsu, H., and M. Ohara. 2003. Genetic diversity and local population structure of fragmented populations of Trillium camschatcense (Trilliaceae). Biological Conservation 109, 249–258.

12. Donovan, T.M., Thompson, F.R., Faaborg, J., Probst, J. 1995. Reproductive success of migratory birds in habitat sources and sinks. Conservation Biology. 9 (6),1380–95.

13. McKinney, M.L. and Lockwood, J. L.. 2001. Biotic Homogenization: A Sequential and Selective Process. In: Biotic Homogenization. New York: Kluwer Academic/Plenum Publishers. 1.

14. Olden, J.D., Poff, N.L., Mckinney, M.L.. 2006. Forecasting Faunal and Floral Homogenization Associated with Human Population Geography in North America. Biological Conservation. 127 (9), 261-271.

15. Ahrné K, Bengtsson J, Elmqvist T. 2009. Bumble Bees (Bombus spp.) along a Gradient of Increasing Urbanization. PLoS ONE 4(5): e5574.

16. McKinney, M. 2006. Urbanization as a Major Cause of Biotic Homogenization. Biological Conservation. 127, 247-260.

17. D’Antonio, C., Meyerson, L.A., 2002. Exotic plant species as problems and solutions in ecological restoration: a synthesis. Restoration Ecology 10, 703–713.

18. Grimm, N.B., Faeth, S.H., Golubiewski, N.E., Redman, C.L., Wu, J., Bai, X., Briggs, J.M. 2008. Global Change and the Ecology of Cities. Science. 319, 756-760.

19. Blair, R.B., 2001. Birds and Butterflies Along Urban Gradients in two Ecoregions of the United States: is Urbanization Creating a Homogeneous Fauna. In: Lockwood, J.L., McKinney, M.L. (Eds.), Biotic Homogenization. Kluwer Academic/Plenum Publishers, New York, pp. 33–56.

20. Niemelä, J. 1999. Is there a need for a theory of urban ecology?. Urban Ecosystems. 3, 57–65.

21. Thompson K, Austin KC, Smith RM, Warren PH, Angold PG, Gaston KJ (2003) Urban domestic gardens (I): putting small-scale plant diversity in context. Journal of Vegetation Science 14, 71–78.