Pollution and phenology

The most alarming of all man's assaults upon the environment is the contamination of air, earth, rivers, and sea with dangerous and even lethal materials. This pollution is for the most part irrecoverable; the chain of evil it initiates not only in the world that must support life but in living tissues is for the most part irreversible. - Rachel Carson

The above quote is taken from Carson's Silent Spring, published in 1963 but sadly still relevant today. Arguably, climate change has overtaken pollution as a concern for the environmentalism movement.

I was wondering about other environmental changes associated with urbanisation which led me to consider the effect of car exhaust fumes on phenology. Vehicular emissions are the major source of air pollution in urban environments (Brophy et al. 2007). These are mostly made up of nitric oxide (NO) and nitrogen dioxide (NO₂).

Car exhaust fumes. Source: the times

Honour et al. (2009) simulated air pollution in roadside, urban environments using a diesel generator fumigation system to see the effect it would have on some herbaceous plants. Their fumigation system emitted lots of different chemicals, not just one or two, which made it like pollution in a real urban environment. Their study was carried out for 3 years. Overall, they found that senescence was brought forward and flowering was delayed compared with the control group.

Hieracium pilosella. Source: wikipedia

Traffic is also a major contributor to heavy metal contamination in soils in urban and roadside environments (Zereini et al., 2007). Ryser and Sauder (2006) found that heavy metal contamination of soils delayed flowering phenology in Hieracium pilosella. They found that flowering phenology was highly sensitive to metal contamination, being affected at very low levels.

Urbanisation (again)

I found a study by Dominoni et al. (2013) which looked at the reproductive phenology of blackbirds (Turdus merula) (Fig. 1) and how this is affected by artificial light. They found that birds affected by night light developed their reproductive system and moulted earlier than those which were not exposed to light. I was interested in this because they used experimental conditions to determine the effect of artificial light, so we can be sure that it wasn't temperature having the effect.

Fig. 1. Male blackbird. Source: http://shropshirebirder.co.uk/blackbird.html

I was thinking there are probably many unaccounted for factors in studies the effects of urbanisation on phenology. Wherever there is a city there will be increased temperatures, light pollution, sources of food, pollution... I'm struggling to find papers that actually separate these effects.

For instance I found this paper by Schoech and Bowman (2008) looking at the reproductive phenology of Florida Scrub-Jays (Aphelocoma coerulescens) (Fig. 2). Those birds from suburban habitats breed sooner in the year. I wrote about how this is makes animals more competitive in a previous post. The authors measured plasma levels of protein, etc. in birds and found it to be higher in the suburban birds vs the rural birds. They inferred from this that earlier breeding is caused by the availability of protein. I think it's good evidence for differences in diet between the two populations. And, they've collected data showing that breeding phenology varies between the two populations. Their results are consistent with their hypothesis that food availability would cause earlier breeding. But, I don't think that necessarily proves the connection because any field study like this will be too confounded.

Fig. 2. Florida Scrub-Jay. Such a beautiful bird! Source: http://barbrichphotography.blogspot.co.uk/2011/05/backyard-birding.html

In fact, the authors found that leutanizing hormone was also elevated in birds. Leutanising hormone is part of the reproductive physiology of birds, the cycle of which is connected to day length (Sharp et al. 1998). Maybe light pollution could have something to do with it, too?

Urbanisation - light pollution vs urban heat island

Light pollution and the urban heat island are both associated with urbanisation. Since blogging about these I've been wondering how studies can be sure they're really seeing the effect of one or the other on phenology.

During winter birds need to get up early to start feeding, as they use their energy up overnight, and need to eat or they'll die of starvation. Ockendon et al. (2009) separated the urban heat island from effects of light pollution by hypothesis testing. In urban areas, they could get up later if it's warmer because they won't have used as much energy up over night staying warm, or they could get up earlier and start feeding sooner because there are artificial sources of light. They found birds appearing at garden feeders later in the a.m. in urban areas in Britain than in rural ones - pointing towards the urban heat island. They also found a statistically significant difference between the response of species, something you might expect if you've been following this blog. They thought the Eurasian collared dove might be getting up to feed earlier because of competition from feral pigeons (Fig. 1).

Fig. 1.

Time between first light and a bird being seen at a feeder (time relative to start; TRS) for the ten most commonly seen species. From Ockendon et al. (2009)

They used modelling to show that urbanisation, defined as the percentage of the surrounding 1 km square classified as urban/suburban, is statistically significant as a predictor variable for time of first bird arrival. However, they did not separate the effects of light pollution and temperature...

Phenology and light pollution (part 2)

Part 2!

Plants
Currently there are no studies on plant phenology and light pollution (Neil and Wu,2006). Although I found this dodgy paper on light pollution impact on tree autumn phenology that reads like it was written by a child and hasn't got proper references

Moths
van Geffen et al. (2014) found that artificial light causes the male Mamestra brassicae (Fig. 1) caterpillar to pupate earlier, The females don't experience this. Differences in pupation duration are strong - by the time the adult moths from the control sample (dark) emerged, after 110 days, ~85% the light polluted moths had already emerged.

Fig. 1 Mamesra brassicae moth

I think there is generally not as much research on light pollution and phenology as compared with temperature and phenology.

Phenology and light pollution (part 1)

We've heard about the Urban Heat Island effect before where plant phenology is affected by increased temperatures around urban areas. But, different species' phenologies are affected by many factors other than temperature. In this post and the next one I'll look at how light pollution can affect phenologies (Fig. 1).

Fig. 1 From Light Cities: Sea Level by David Stephenson (2012)

Birds
Light pollution can affect bird migration, but can't really affect the timing (phenology). Interestingly, some migratory birds are guided by stars in the night sky, and light pollution confuses them on their way and they can collide into each other and die (Longcore and Rich, 2004; Poot et al., 2008)!

Zooplankton
Aquatic invertebrates move up and down the water column in response to changing light conditions over 24 hours, something called "diel vertical migration" (Gliwicz 1986; cited in Longcore and Rich, 2004). Daphnia is an aquatic invertebrate (Fig. 2). Moore et al. (2000 cited in Longcore and Rich, 2004) found that the range of its diel vertical migration is affected by artifical light sources.

from http://www.micromagus.net/microscopes/pondlife_cladocera.html

More next time...

Phenological changes and mankind

This post will look at some of the impacts phenological changes can have on mankind, and whether these are good or bad.

"Ecosystem services" are the benefits people gain from ecosystems. They can be split up into into provisioning, regulating, cultural and supporting services (Fig. 1).

Fig. 1 Examples of ecosystem services by type. Taken from unep.org.

Provisioning services

Pelagic plankton and fish in the North Sea show phenological changes in response to warming sea surface temperatures, but their responses are mismatched in time (Edwards and Richardson, 2004). We've heard about decoupling between trophic levels before. In this context, these phenological mismatches could detrimentally effect fisheries, because the success of fish depends on their synchronisation with growth of plankton (because they eat them).

Regulating services

We've heard before that the growing season is lengthening. A longer growing season in northern Europe (Fig. 2) could be beneficial for agricultural yields and insect populations, and allow us to introduce crops to new areas where they previously could not grow (LaValle et al., 2009).

 

Fig. 2. Rate of change of crop growing season 1975-2007. Taken from LaValle et al. (2009).

However, again, there is concern that there could be mismatches in the phenology of flower production and pollinator flight activity. Memmott et al. (2007) used phenological data from 1884 - 1916 on the first and last dates of flowering, and visits from pollinators, to predict what would happen to plant-pollinator interactions in a simulation of future global warming for the years 2070-2100. They found that most pollinators would be at risk in this scenario, and that local extinction of pollinators will put plant sexual reproduction at risk, and cause plant populations to decline.

Cultural services

Ecotourism has explicit links with plant phenology:

"...autumn tourists, including “leaf peepers”, are estimated to spend US$375 m in Vermont alone ... In Japan, both autumn colour watching (“momijigari”) and viewing of spring flowers (“hanami”) are hugely important; 10 million visitors a year visit the famous 59-ha Arashiyama National Forest near Kyoto ... and when cherry flowering coincides with public holidays this attracts an additional 1.4 million tourists to Hirosaki... Cherry flowering is also a huge attraction in Korea, China and across North America where an estimated 700,000 visitors visit Washington D.C. for the cherry blossom festival..." - Sparks et al. (2012; p. 1)

Sparks et al. (2012) looked at the spring snowflake (Leucojum vernum) (Fig. 3) which the flowering of is a tourist attraction in Poland. They found that earlier flowering was associated with a long flower duration. This would be beneficial for ecotourism.

Fig. 3. Spring snowflake blossom heralds the start of spring. Source: http://www.panoramio.com/photo/68598215

This is all well and good. But ecosystem services frame the biosphere as valuable only because it provides mankind with something, rather than respecting life for its intrinsic value.

Delayed autumn senescence

from https://www.flickr.com/photos/andrewsteele/4082262513https://www.flickr.com/photos/andrewsteele/4082262513

The growing season at mid-to-high latitudes has been lengthening as a result of climate change. This is primarily due to an advancement of spring, but it's also partly due to a delay in autumn phenologies (IPCC, 2007). Indeed, we're having quite a mild autumn this year, and it seems natural to conclude that this would cause leaves to retain their leaves for longer, and to change colour later. However, changes in autumn phenologies are less well understood than spring ones. I touched on this in my previous post. Advancing spring phenologies correlate well with rising temperatures, but delayed autumn phenologies correlate less well, which implies that there are other factors playing a role.

Similarly to some instances of bird migration and mammal hibernation, in many trees, growth cessation, the first stage in winter dormancy, is initiated by day length (Wareing, 1956). It was thought that Populus' autumn phenologies are controlled by photoperiod. But Taylor et al. (2007) performed an experiment where Populus trees were grown with elevated CO2 (550ppm, we're now at ~400ppm) and found that this delays autumn leaf colour changes and leaf fall. Rhode at al. (2011) found that Populus trees also found that temperature had an effect. However, these studies are all done on one species and it's fairly certain that there will be species-specific responses to the same environmental changes.

Mammals

Studies of changes in phenology in response to climate change have focused particularly on migratory birds, since they may be more likely to experience mismatches between their time of arrival and the coming of spring in their breeding grounds (see previous post). What about mammals? Let's have a look at a couple of studies.

Hibernation. Like migratory birds’ migrations, hibernation is controlled by “endogenous rhythms” – i.e. an innate response to day length. However, mammals are able to alter the phenology of their hibernation in response to climate change, through “phenotypic plasticity” - i.e. one genotype can produce different phenotypes depending on environmental conditions.  Over longer timescales, it’s likely that microevolution of phenological traits will be more important for species to survive. 

Reproduction. Chillingham cattle are a rare breed of cattle. A wild population roams in Northumberland and there are records of their births and deaths since the 1860s. This breed gives birth throughout the year, but it’s been found that they’ve been having more calves during the winter. Weather data points to warmer springs as the reason: the cattle have a 9 month gestation period, and have been conceiving earlier because of an earlier availability of vegetation for food. This is bad news, because winter born calves don’t do as well.

Stay posted for more fascinating phenological facts ;)

Birds of Britain...

Reproductive phenologies, biotic interactions, and when things go wrong….

Animals need to synchronise their reproductive phenologies with the seasonal availability of resources, so that they’re reproducing at the time of maximum resource abundance. Plants and insects have advanced their spring phenologies as spring temperature has increased. The animals which rely on them for food need to advance their reproductive phenologies in step, in order to cope with this change.

Migratory birds have been heavily studied in this regard. Some species have not advanced their timing of breeding. Unsurprisingly, European migratory bird species which advanced their spring migration phenology in the past decades have stable or increasing populations, but those which have failed to respond have decreasing populations.

The migratory pied flycatcher, Ficedula hypoleuca, is one example. It has had trouble adapting to climate change because the timing of its migration is controlled by “endogenous rhythms”, such as day length, which are not affected by climate change. The pied flycatcher populations with the largest declines are those where its prey’s population peaks early in the spring – because it hasn't been arriving earlier, it’s missed the time of peak food availability. When prey population peaks later, the birds do better. 

Pied flycatcher pic from BBC

Land surface phenology

Phenology has traditionally used data collected on individual organisms, or species. “Land surface phenology” uses satellites to monitor the phenological status of vegetation from space. This is a different kind of data: satellites provide a continuous record of the pattern of every number of phenological processes as an aggregation of a large area of land.

One of the applications of land surface phenology has been the study of the urban heat island effect, where urban areas are warmer than rural areas. Zhang et al. (2004) used satellite data to look at vegetation phenology in eastern North America. They found that, on average, the growing season lengthened by 15 days surrounding urban areas compared with rural ones. This was because of an earlier onset of green-up by 7 days, and a later onset of dormancy by 8 days. The difference in green-up was a largely function of temperature, which is elevated around urban areas. However, dormancy is more complicated, and probably has more to do with a variety of factors such as water availability and day length. They also found that the difference was detectable up to 10km away from the edge of urban areas.

Greenup (ΔG) comes earlier and dormancy onset (ΔD) comes later around the urban areas of Washiungton DC, New York and Boston. Temperature is elevated around urban areas in spring (ΔLST_1–5), and in autumn/winter (ΔLST_9–12). From Zhang et al. (2004).

A diverse vegetation phenological response to climate change has also been detected using remote sensing. Bunn and Goetz (2006) looked at trends in photosynthesis for 22 years of satellite measurements in the northern circumpolar high latitudes. Warming would be expected to cause vegetation growth, as with the urban heat island effect. The treeline has also been observed to be migrating northwards because of global warming. However, they found that 85% of the areas they studied showed no change. Moreover, of those areas that did show change, tundra areas experienced increases in photosynthesis (“greening”), but boreal forest areas experienced decreases (“browning”). It could be that increases in evaporation in the Arctic is causing drought stress that trees cannot cope with, leading to browning, despite global warming.

Changes in photosynthetic activity in northern circumpolar areas in early and late summer. Red and yellow areas are mostly tundra and show a greening trend. Blue areas are mostly boreal forest and show a browning trend. Most areas show no difference and are lilac. From Bunn and Goetz (2006).

These results are not entirely straightforward: phenology is not limited to the observation that 'spring is coming sooner'! Phenological phenomena - autumn senescence around urban areas, and photosynthetic activity in boreal forests - are not solely a function of temperature. But a complicated world is more interesting than a simple one. :)

Welcome to the Anthropocene

In its 4.6 billion year history, the Earth has always been in a state of flux: various astronomical, geological, and biogeochemical forces have driven dramatic and almost unimaginable changes in the Earth’s environment. I would love to go back in time and see a completely alien Earth with lush tropical forests at the poles about 55 million years ago, or to somehow watch a time-lapse from the moon of huge ice sheets coming and going over the surface of the Earth over hundreds of thousands of years!

Since humans evolved some 200,000 years ago, and as our populations and enterprises have grown, we’ve been leaving more and more of a mark on this world. In fact, the sheer pace and magnitude of recent, human-induced environmental change is so dramatic that it overshadows natural forces we observe in the geological record. This has led scientists to propose a new epoch - that is, coin a new term for our time - the Anthropocene.

The human impact on the environment is not limited to global warming, but that's what grabs everyones attention. What is happening, and will happen in the future, to plants and animals during this time of rapid warming?

There are numerous ways in which species can potentially respond to environmental change. On long timescales, they can evolve. They can go extinct. They can move away, to a more suitable habitat. Or, they can show changes in their phenology.

Phenology is the study of the timing of seasonal plant and animal activity. The oldest phonological records date from AD 705 Japan, and are of the first cherry blossoming. Robert Marsham has been called the founding father of phenology. From 1789 he made meticulous records of, for example, the first frog and toad croaks, first snowdrops, and first turnip flower to appear. He kept these records up for decades, and successive generations of the Marsham family maintained the tradition. Nowadays anybody can submit their observations online. Modern technology is a blessing, letting us amass such large datasets.

Plenty of people have casually observed that spring is coming sooner. In fact, studies have shown that spring has been advancing by 2.3-5.2 days per decade for the last 30 years, and there is good evidence to show that this is caused by recent warming.

In this blog I'll be exploring current research in phenology. Plants and animals are inherently interesting, but the details of scientific papers can sometimes be a bit inaccessible to the layperson (and to students!!!). I hope to learn a lot, and I look forward to showing this blog to my friends and family. Until next time!