Australasian Science Magazine

Frogs have to adjust their calls in order to be heard in noisy urban environments. Credit: Matt Clancy Wildlife Photography (CC BY 2.0)

By Bob Wong

Sex isn’t always easy, but it’s becoming a lot more complicated due to human-induced changes to the natural environment.

Nestled near the mouth of the Irwin River, some 350 km north of Perth, lies the tiny coastal community of Dongara – the self-proclaimed rock lobster capital of Australia.

Three decades ago, in bushland just outside of town, it was an altogether different kind of creature that attracted the attention of scientists: male beetles (Julodimorpha bakewelli) had developed a sexual predilection for discarded beer bottles. The beetles were drawn to the shiny brown surface and textured patterns of the empty stubbies, which bear a striking resemblance to the shiny brown elytra, or hardened forewing, of female beetles (except beer bottles are substantially larger, and therefore sexier, than actual females). So persistent were the male beetles’ attempts at copulating with the empty bottles that some were falling prey to predatory ants biting at the soft portions of their genitalia.

While bottle-loving beetles may, at first, seem a little amusing, such behaviours highlight the challenges of sex in an increasingly human-altered world.

The Quest for Sex

Securing a suitable mate, even at the best of times, can pose a significant challenge for sexually­ reproducing organisms. Charles Darwin’s On the Origin of Species described it as a sexual struggle arising from intense competition among individuals for the opportunity to mate. This struggle is so powerful that it can shape the course of evolution itself. Indeed, many of the most spectacular and complex traits and behaviours found in nature – from the tail of the peacock to the claw-waving display of fiddler crabs – stems from this process, which Darwin coined “sexual selection”.

Spectacular and showy they may be, but sexy traits are also costly to produce and maintain. Colourful displays can be time-consuming and energetically taxing to perform, not to mention dangerous in terms of attracting unwanted attention from would-be predators. Evolutionary theory predicts that only individuals in the best condition should be able to bear the cost of producing the most exaggerated sexual signals, which are, in turn, relied upon by choosy members of the opposite sex to select the best mates.

But exaggeration requires a context, and sexual signals are often finely attuned to the local environmental conditions in which they have evolved. So what happens when environmental conditions are altered as a result of human activities?

Masquerading in Murky Waters

Humans have caused dramatic and widespread changes to environments worldwide. Such changes can affect sexual selection by altering the signalling environment, and hence the effectiveness of sexual traits and behaviours important in mate attraction.

An example of this is seen in aquatic habitats, where an increase in nutrient input – mainly from agricultural, industrial and urban sources ­– can fuel the rampant growth of algae, which reduces visibility in the water column. By making the water murky, algal blooms influence colour perception in several species of fish, potentially undermining the value of visual signals that are important in mate attraction and species recognition.

One of the best-known examples of this comes from work carried out in East Africa. Researchers studying the cichlid fishes in Lake Victoria found that reduced visibility led to accidental matings between closely related species, which were unable to tell each other apart in all the murkiness. This led to the breakdown of an important mechanism (i.e. colour) that was helping to maintain the integrity of species within the Lake – resulting in the loss of biodiversity.

Sex and the City

It is not only visual signals in degraded aquatic habitats that are affected. Increased urbanisation represents a significant challenge for many terrestrial animals. The growth and expansion of cities around the globe is occurring at an unprecedented rate, with predictions that as much as 60% of the world’s human population will be living in urbanised landscapes by 2030.

For urban-dwelling animals that rely on calls to attract their mates, the persistent low-frequency noise in urban environments can make it difficult for individuals to be heard. Tall buildings exacerbate the problem by ricocheting sound and, in so doing, further distorting and degrading acoustic signals.

In noisy urban environments, animals need to find ways to prevent their calls from being muffled if they are to communicate effectively. One way to achieve this is to adjust the frequency of their calls above the din of human-generated noise.

A number of studies have reported such frequency shifts in the songs of urban-dwelling birds. Research in Australia, for example, show that birds in cities often sing at higher frequencies compared with their rural-dwelling counterparts.

Similar cases of vocal adjustments have also been reported in urban-dwelling frogs. Like songbirds, male frogs rely on calls to attract females for mating. Recent research on the southern brown treefrog (Litoria ewingii), for example, showed that city-dwelling males call at higher frequencies in order to be heard over urban traffic.

Apart from changes to the frequency of their calls, acoustically-communicating animals can also make adjustments in other ways. A study on silvereyes (Zosterops lateralis) in south-eastern Australia, for instance, showed that urban-dwelling birds sing more slowly than their rural conspecifics, with fewer syllables per second. The researchers speculate that urban silvereyes, by adjusting the structure of the song itself, are able to counter the effect of signal degradation that would render faster, more complex songs indecipherable.

Despite evidence that animals are able to adjust their signals in response to altered conditions, it remains unclear how changes, such as those reported in urban-dwelling birds and frogs, might affect their reproductive success. In birds, song and syllable complexity affect the attractiveness of the singer. Similarly, female frogs prefer males that produce lower-pitched calls.

Hence, if animals are forced to produce less complex or higher pitched calls in noisy environments, such adjustments could potentially result in a conflict between audibility to prospective suitors as well as the attractiveness of the caller. Such a possibility, however, remains to be tested.

Gender Bender

Chemical pollution can also have direct and negative impacts on reproduction. Over the last few decade, one particular group of environmental pollutants has attracted particular concern. Known as endocrine-disrupting chemicals (EDCs), these widespread contaminants enter the environment through a variety of sources, from discharge of household wastewater to agricultural run-off and industrial effluent. They encompass a diverse range of natural (e.g. hormones present in urine and faeces of livestock) and synthetic compounds (e.g. plastics, pesticides and pharmaceuticals) that block or mimic the effects of hormones, thereby stimulating or inhibiting the endocrine system. EDCs have become ubiquitous in the environment and are commonly found in the tissues of wildlife and humans – even in the most remote regions on earth (e.g. polar bears in the Arctic).

In Australia, endocrine disruption is a growing health and environmental issue – underscored by recent health warnings against the consumption of tainted seafood and concerns over the contamination of drinking water supplies. In particular, Australian freshwater environments, like those in many other parts of the world, are common repositories for the discharge of large volumes of domestic and industrial waste. Recent research suggests that our intensive agricultural practices also contribute significantly to EDC pollution of Australia’s waterways, especially in rural areas, where concentrations of some EDCs have been detected at levels comparable to those found in effluent from wastewater treatment plants.

In the context of reproduction, EDCs cause a wide range of developmental and physiological problems, from egg shell thinning in birds to the development of abnormal genitalia in alligators – a sure-fire way to complicate sex. EDCs also induce alarming changes to reproductive behaviour, a fact first brought to the attention of the scientific community more than five decades ago in a landmark study linking pervasive use of the pesticide DDT with altered nesting and courtship behaviours in American bald eagles. Since then, our understanding of the behavioural impacts has advanced surprisingly little.

Recently, however, a study on laboratory mice showed that exposure to EDCs can affect female mating preferences that can persist across multiple generations. The implications of this are far-reaching. If exposure to EDCs can induce changes that transcend generations, contamination of habitats by EDCs need not be permanent to have long-lasting reproductive effects.

Trash and Treasure

Human-induced changes to the environment aren’t always bad when it comes to reproduction. Indeed, individuals of some species may even exploit altered environmental conditions to maximise their chances of mating.

A prime example is seen in bowerbirds, which are known for their spectacular and colourful courtship displays involving the use of decorative objects and purpose-built bowers. The bowers themselves reveal important information to discerning females about the quality of the builder. Male bowerbirds living in close proximity to humans readily incorporate rubbish objects, such as colourful bits of plastics and glass, into the courts of their bowers as decorations to attract females.

Other examples of nest adornment have also been reported in birds of prey, with black kites (Milvus migrans) in Europe using white plastic bags in their nest as a signal of the builder’s fighting prowess and to ward off intruders. Clearly, not all species are adversely affected by change.

Conclusion

Human habitat modifications and their impacts on biodiversity pose an urgent challenge to biologists. Given the unprecedented scale of human-induced changes to ecosystems worldwide, it is critical to understand why some species flounder while others thrive.

As we have seen, changes to the environment can influence how animals communicate and with whom they end up mating – if they end up mating at all. Thus, by influencing reproductive outcomes and, hence, the number and quality of offspring produced, sexual selection can be important in determining the fate of populations and, ultimately, the persistence of species in a rapidly changing world.