The University of Southampton

Plants in Elevated CO2: Stimulated Photosynthesis, Good News or Bad News?

Climate change, I believe people are familiar with this word, although some of them may not believe it, it is the truth that is happening right now.

Since the Industrial Revolution, a large amount of CO2 has been released into the atmosphere due to the burning of fossil fuel. Human has obtained great development from Industrial Revolution and we are living a better life. However, the increasing concentration of CO2 in the atmosphere is warming our planet! We already know that the high temperature, extreme weather and sea level rise are the horrible consequences of climate change, but what about the impacts on plants?

Plants are the major terrestrial carbon sink. They absorb CO2 and water as raw materials, use sunlight as the energy source, release O2 and store sugars in organs as products, which support the plant growth and fix carbon in the wood and leaves. This process happens in the tiny chloroplast inside the cells of leaves and is called photosynthesis, which is a crucial chemical reaction on the earth, as oxygen is essential to human life.

The process of Photosynthesis

The process of Photosynthesis. (Patrickodonkor, 2017)

It seems that the increasing atmospheric concentration of CO2 provides the plants more CO2 input. Will it stimulate the photosynthesis process of plants? Probably. Some studies show that plants increase the photosynthesis rate in the elevated CO2 concentration, and especially, more evidence is found for the C3 plants (plants grow in the cool, wet climate) (Kirschbaum, 2004).

Although the plants may be happy with taking in more carbon for their growth and development, the Rubisco, which is the most abundant protein playing a role in the photosynthesis, seems unhappy with the elevated CO2. The activity of Rubisco decreases, and the Rubisco content shows a 20% drop in the elevated CO2 condition (Long et al., 2004). Such change is the acclimation of plants to the changing environmental condition, and the elevated CO2 decreases the photosynthesis capacity in long term.

However, even with the acclimation of photosynthesis capability, significant enhancement of carbon uptake has been found in the Free-Air Carbon dioxide Enrichment (FACE) studies of plants grow in the exposure to the CO2 concentration of estimated mid-century scenario (Leakey et al., 2009). This may be a good news, as the plants absorb more CO2, they can somewhat offset the greenhouse emissions and slow down the climate change. Moreover, the dry matter production and seed yield of C3 plants also slightly increased, although it is not as significant as the increase of carbon uptake (Long et al., 2004).

Another general finding of plant’s response to elevated CO2 is the increasing nitrogen use efficiency of photosynthesis. As the Rubisco decreases, less nitrogen is needed and the C: N ratio increases (Drake, Gonzàlez-Meler and Long, 1997). That is to say, the elevated CO2 reduce the nitrogen content in plant tissue and thus fewer nutrients are provided by the plants (Cotrufo, Ineson and Scott, 1998). People have to consume more food than before to obtain the same amount of nutrients!

Can you accept this trade off?

[493 words]

 

Reference

  • Cotrufo, M., Ineson, P. and Scott, A. (1998). Elevated CO2 reduces the nitrogen concentration of plant tissues. Global Change Biology, 4(1), pp.43-54.
  • Drake, B., Gonzàlez-Meler, M. and Long, S. (1997). MORE EFFICIENT PLANTS: A Consequence of Rising Atmospheric CO2?. Annual Review of Plant Physiology and Plant Molecular Biology, 48(1), pp.609-639.
  • Kirschbaum, M. (2004). Direct and Indirect Climate Change Effects on Photosynthesis and Transpiration. Plant Biology, 6(3), pp.242-253.
  • Leakey, A., Ainsworth, E., Bernacchi, C., Rogers, A., Long, S. and Ort, D. (2009). Elevated CO2 effects on plant carbon, nitrogen, and water relations: six important lessons from FACE. Journal of Experimental Botany, 60(10), pp.2859-2876.
  • Long, S., Ainsworth, E., Rogers, A. and Ort, D. (2004). RISING ATMOSPHERIC CARBON DIOXIDE: Plants FACE the Future. Annual Review of Plant Biology, 55(1), pp.591-628.
  • Patrickodonkor, (2017). Process of photosynthesis. [online] YouTube. Available at: https://www.youtube.com/watch?v=krat2mnM1M0 [Accessed 19 Mar. 2017].




Humanity must stop neglecting changes in Seagrass Meadows before disaster?

Seagrass meadows are a vital habitat and food source for many endangered species but these crucial habitats are under threat from environmental change caused by human impacts climate change, coastal developments, fishing and aquaculture (Waycott etal, 2009).

Figure 1- Manatee feeding on seagrass (USGS, 2016)
Figure 1- Manatee feeding on seagrass (USGS, 2016)

Climate Change

Climate change will cause a wide variety of impacts on the oceans which will effect seagrasses increasing water temperatures will lead to increased instances of seagrass die off, ocean acidification caused damaged to the cells plants require to photosynthesize and grow (Repolho et al, 2017).

As seagrass requires shallow habitats as sea levels rise there will be a loss of seagrass in deeper areas of their range seagrasses will move shoreward this trend is similar to trends that are being seen from increased amounts of sediments within the water as they will lack the sunlight to photsynthesise (Davis et al, 2016).

Coastal Developments

The construction of ports, artificial beaches and the reclamation of land, the adding of material to the water to fill in the area, this leads to more sediments within the water. The increased amount of sediments in the water can lead to seagrass beds being completely buried by the sediment and stopping plants from photosynthesising which it needs to survive, during the construction of the Pointe-Rouge Harbour over 68ha of seagrasses were lost due to water sediment and 11ha destroyed by construction (Boudouresque et al, 2009).

Figure 2- The Light grey shows dead seagrass and the dark grey living seagrass after the laying of a cable between two islands in the South of France (Boudouresque et al, 2009)
Figure 2- The Light grey shows dead seagrass and the dark grey living seagrass after the laying of a cable between two islands in the South of France (Boudouresque et al, 2009)

 

Fishing and Aquaculture

A trawler can uproot between 99,000-363,000 shoots during a trawl and in some areas of the Mediterranean over 80% of the seagrass meadows have been destroyed due to trawling (Boudouresque et al, 2009). Aquaculture, mainly fish farms, can cause a process called eutrophication, an excessive increase in nutrients heading into a body of water leading to high algal growth, because of the nutrients from uneaten food and excretion from the fish as it is focussed in one area around the fish farm this causes the reduction in size of the plants in the area due to reduced light reaching the plants, leading to a regression of the plants in the areas around fish farms (Ruiz et al, 2001).

pic-3
Figure 3- Changes in seagrass area by coastlines and in most coastlines more studies report a decrease (Waycott et al, 2009).

Future of Endangered Species

Dugongs, sea turtles and manatees all directly depend upon seagrass in many tropical regions for food and with decreases in seagrass globally, figure 3, they is likely to be further pressure put onto these already endangered species (Waycott et al, 2009), and if humanity does not take steps to solving the problems mentioned here the future of these iconic species is in real danger.

 

 

Reference List

Boudouresque, C., Bernard, G., Pergent, G., Shili, A., Verlaque, M., (2009), Regression of Mediterranean seagrasses caused by natural processes and anthropogenic disturbances and stress: a critical review, Botanica Marina, 52, 395-418

Davis, T., Harasti, D., Smith, S., Kelaher., (2016), Using modelling to predict impacts of sea level rise and increased turbidity on seagrass distributions in estuarine embayments, Estuarine, Coastal and Shelf Science, 181, 294-301

Repolho, T., Duarte, B., Dionísio, G., Paula, J., Lopes, A., Rosa, I., Grilo, T., Caçador, I., Calado, R. and Rosa, R. (2017). Seagrass ecophysiological performance under ocean warming and acidification. Scientific Reports, 7, p.41443.

Ruiz, J., Perez, M., Romero, J., (2001), Effects of Fish Farm Loadings on Seagrass (Posidonia oceanica) Distribution, Growth and Photosynthesis, Marine pollution bulletin, 42(9), 749-760

USGS, (2016). Manatees [online] Available at: https://www.usgs.gov/centers/wetland-and-aquatic-research-center-warc/science-topics/manatees [Accessed 20 Mar. 2017].

Waycott, M., Duarte, C., Carruthers, T., Orth, R., Dennison, W., Olyarnik, S., Calladine, A., Fourqurean, J., Heck, K., Hughes, A., Kendrick, G., Kenworthy, W., Short, F. and Williams, S., (2009). Accelerating loss of sea grass across the globe threatens coastal ecosystems,. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 106(30), 12377-12381

 

Word Count – 489

 

 

 





How can plants cope with rising temperatures?

crop

A dead crop that has experienced extreme drought Source: Inhabitat.com (2017).

Average global surface temperatures around the world are increasing (Carlowicz, 2010) as a result of increased carbon dioxide in the atmosphere.

temp

Annual average global surface temperatures since the industrial revolution. Source: Climate.gov (2017)

All organisms have a narrow temperature range within which they function best and a broader range they can tolerate. Organisms that can easily move, for example animals, will move to stay within these limits. Plants however are unable to get up and move to maintain these limits in an individual’s life time, though with subsequent generations they can, through seed dispersal (Felde, Kapfer and Grytnes, 2012). But in order to do this they need to survive in the short term.

So the question is how do they do this?

Temperature is one of the most important factors that affects plant development. It controls the rate of most of the reactions occurring inside the plant and increases the storage of sugars inside the plant. As temperatures increase, the impact of the other growth limiting factors become more apparent, especially drought, as higher temperatures increases the rate of transpiration, the process that moves water through the plant.

In general:

Warmer temperatures = Faster Growth + more water consumption

As most gardeners know, extremes of temperature can be deadly. Low temperatures can cause freezing within the plant, which although rare, causes cell death. High temperatures cause not only loss of water and therefore wilting, but with long-term/extreme exposure causes a breakdown of the proteins insides the plant cells (Mathur, Agrawal and Jajoo, 2014), reducing their function, and ultimately causing death. Differences in morphology allow for plants to have varying tolerances to temperature extremes such as fleshy leaves, classic of succulents.

wilted-plant

Healthy plant (left), Wilted plant (Right) Source: Chng, (2017)

 

Temperature also has a very pronounced effect on photosynthesis, the process by which plants produce food. The optimum temperature varies by species and will have adapted to work best in their given environment. The genetics of an organism may also determine the tolerance of temperature change; for example plants containing a specific gene for carbon fixation have a higher tolerance to warm temperatures compared to those who don’t have it. (Berry and Bjorkman, 1980).

Some species such as Eucalyptus pauciflora (Berry and Bjorkman, 1980), have a natural flexibility with optimal temperature for photosynthesis, which closely follows seasonal changes in air temperature. Plants with such natural flexibility will likely more readily adapt to the changing climate.

Pollination and seed development are one of the most temperature sensitive processes in the plant life cycle, but there are very few adaptations to combat this; in an experimental study (Hatfield and Prueger, 2015), the seed development in maize was reduced by 80-90% with increased temperatures. Without mechanisms in place to reduce this effect, it makes it more important for adaptations in other life cycle stages to reduce the impact of temperature variation.

adaptations

A summary of the different techniques plants can use to reduce high temperature stress. Source: Mathur, Agrawal and Jajoo, (2014)

To survive short term plants may employ a variety of techniques shown in the image above. The long term adaptation of maximizing photosynthesis allows plants to make the most of the changing environment, and allows the plant to survive long enough to reproduce.

Word Count:499

 

References

Berry, J. and Bjorkman, O. (1980). Photosynthetic Response and Adaptation to Temperature in Higher Plants. Annual Review of Plant Physiology, 31(1), pp.491-543.

Carlowicz, M. (2010). World of Change: Global Temperatures : Feature Articles. [online] Earthobservatory.nasa.gov. Available at: https://earthobservatory.nasa.gov/Features/WorldOfChange/decadaltemp.php [Accessed 21 Mar. 2017].

Chng, J. (2017). Healthy Wholesome Food ~ Be a WISE Consumer to safeguard your HEALTH. [online] Healthywholesomefood.blogspot.co.uk. Available at: https://healthywholesomefood.blogspot.co.uk/search/label/e%20excel%20orchestra [Accessed 21 Mar. 2017].

Climate.gov. (2017). Why did Earth’s surface temperature stop rising in the past decade? | NOAA Climate.gov. [online] Available at: https://www.climate.gov/news-features/climate-qa/why-did-earth%E2%80%99s-surface-temperature-stop-rising-past-decade [Accessed 21 Mar. 2017].

Felde, V., Kapfer, J. and Grytnes, J. (2012). Upward shift in elevational plant species ranges in Sikkilsdalen, central Norway. Ecography, 35(10), pp.922-932.

Hatfield, J. and Prueger, J. (2015). Temperature extremes: Effect on plant growth and development. Weather and Climate Extremes, 10, pp.4-10.

Inhabitat.com. (2017). Fungus-Infused Superplants Could Survive Forthcoming US Droughts. [online] Available at: http://inhabitat.com/fungus-infused-superplants-could-survive-forthcoming-us-droughts/dead-crops/ [Accessed 21 Mar. 2017].

Mathur, S., Agrawal, D. and Jajoo, A. (2014). Photosynthesis: Response to high temperature stress. Journal of Photochemistry and Photobiology B: Biology, 137, pp.116-126.





UK Food in a climate crisis?

British food security is under threat due to Climate change.

If you haven’t heard of ‘climate change’ you‘ve either been living under a rock for the last 30 years or getting yourself elected as leader the free world. But not much has changed, Winter’s a little warmer, summer’s a little wetter? We’ve heard of extreme weather conditions in some far corners of the globe but unless you’ve been planning a trip there, it’s unlikely to affect our everyday lives. But behind supermarkets sliding doors lurks a real peril, one directly impacting Britons at their most vulnerable part, our Achilles heel, our pockets. As crop production is jeopardised, already inflated prices are set to rise, correlating with the environmental changes induced by human pollution (Lobell, 2007).

Figure 1. A familiar slight, well stocked fruit and veg for public consumption. But for how long? (WordShore (flickr), 2016)
Figure 1. A familiar slight, well stocked fruit and veg for public consumption. But for how long? (WordShore (flickr), 2016)

Food security is perhaps the most important commodity provided by the planet. At a glance the effects of climate change, seem on the whole, to be exactly what farmers are looking for in terms of improving yield from their crops. It’s wet, hot, there’s more CO2, more decomposition and available nutrients, just what plants need right? But this is not always the case, although higher CO2 levels does stimulate plant growth, it is counteracted by the increase in temperature and ozone, a molecule with harmful effects on plant tissue(Hogsett, et al 1997). Warming decreases the quality of the crops produced, grains are less dense and seeds contain less oil, as well as favouring growth and proliferation of weeds into new areas, due to the differences in how they photosynthesise (Fuhrer, 2003. Martre, 2017).

Figure 2. The graph from DEFRA (Department for Environmental Food and Rural Affairs) shows billions of pounds worth of imported food, especially fruit and vegetables. (Source: DEFRA Food Statistics Pocketbook 2016)
Figure 2. This graph from DEFRA (Department for Environmental Food and Rural Affairs) shows billions of pounds worth of imported food, especially fruit and vegetables. (Source: DEFRA Food Statistics Pocketbook 2016)

It is no secret that as a nation we currently import almost half of our food and animal feed from overseas (Ruiter et al 2015). In response to huge population increases of 3 Million on average every decade since the baby boomers of the 50s(Humby, 2016) and market for year-round exotic produce. But tropical regions are likely to suffer much more, even a slight temperature increase interfering with developmental and growth processes beyond already stretched thresholds, meaning production in these areas will fall hugely(Challinor, 2008). Excess precipitation, effectively drowning roots and drought adding another uncertain dimension to the mix(Amedie, 2013).

“[In staples like wheat, maize and barley] warming has resulted in annual combined losses of $5 billion per year, as of 2002” -Lobell, 2007

Environmental change is going to effect everyone in one way or another, we rely on plants for food, clothing, oxygen, medicine and much more. Prices of everyday commodities reflect the quantity and quality of production processes. The result is innumerable aspects of our lives being changed, in some way by the unsustainable practices we are complicit to on a daily basis(Lepetz et al., 2009).

Research into genetic modification of crop plants provides some relief in the challenges ahead, improving crop plant coping mechanisms and yield potential (Martre et al 2017), as well as a decrease in the consumption of animal products due to their high carbon footprint and inefficiency(Ruiter et al 2015). For now it will be a 4p increase in a farmhouse loaf and 10p extra for sunflower oil, but immediate action is necessary to prevent a large-scale food shortage in the near future.

[500 words]

References:

Amedie, F.A., (2013). Impacts of Climate Change on Plant Growth, Ecosystem Services, Biodiversity, and Potential Adaptation Measure. , pp.1–61.

Challinor, A.J. & Wheeler, T.R., (2008). Crop yield reduction in the tropics under climate change: Processes and uncertainties. Agricultural and Forest Meteorology, 148(3), pp.343–356.

Fuhrer, J., (2003). Agroecosystem responses to combinations of elevated CO2, ozone, and global climate change. Agriculture, Ecosystems and Environment, 97(1–3), pp.1–20.

Hogsett, W.E., J.E. Weber, D. Tingey, A. Herstrom, E.H. Lee and J.A. Laurence. (1997). An approach for characterizing tropospheric ozone risk to forests. Environmental Management 21:105-120.

Humby, P. (2016). Overview of the UK population: February 2016. [ONLINE] Available at: https://www.ons.gov.uk/peoplepopulationandcommunity/populationandmigration/populationestimates/articles/overviewoftheukpopulation/february2016. [Accessed 13 March 2017].

Lepetz V., Massot, M. & Schmeller, D.S., & Clobert, J., (2009). Biodiversity monitoring: some proposals to adequately study species’ responses to climate change. Biodiversity and Conservation 18, 3185- 3203

Lobell, D.B. & Field, C.B., (2007). Global scale climate–crop yield relationships and the impacts of recent warming. Environmental Research Letters, 2(1), p.14002.

Martre, P., Yin, X. & Ewert, F., (2017). Modeling crops from genotype to phenotype in a changing climate. Field Crops Research, 202, pp.1–4. Available at: http://linkinghub.elsevier.com/retrieve/pii/S0378429017300242.

Ruiter, H. de et al., (2015). Global cropland and greenhouse gas impacts of UK food supply are increasingly located overseas. Journal of The Royal Society Interface, 13(114). Available at: http://rsif.royalsocietypublishing.org/content/13/114/20151001.abstract.

WordShore (flickr), (2016), Fruit (WordShore)[ONLINE]. Available at: https://hiveminer.com/Tags/hebrides,solas [Accessed 15 March 2017].





It’s getting hot in here! Can plants handle global warming?

Looking at the potential future impacts of climate change on global plant life                                     By Catherine Savage, University of Southampton student


The human race is turning over a new leaf – but not in a good way.

As we enter a new era, the Anthropocene, what will be the fate for plant life on earth?

plant
Source: Better globe AS, Copyright © 2017.

 

Everyone knows what climate change is, everyone knows that it is a current hot topic, but does everyone know what is happening to our plants because of it?

Global temperatures have risen 0.9 degrees throughout the last century (IPCC, 2013). This is predicted to rise by 4 degrees before 2100 (Thuiller, 2007).  A shocking reality to grasp, yet global temperature change is only one aspect encompassed in the concept of climate change.  What about changes in rainfall? Ice sheet melting? Sea level rise?

So, what are the underlying causes of climate change? Out of the greenhouse gases, carbon dioxide contributes the most to global warming at 65%. Current carbon dioxide concentration in the atmosphere is 387ppm, exceeding the safe level of 350ppm (Hansen et al., 2015). This has been heightened by fossil fuel burning and land-use change. The extra CO2 increases the greenhouse effect, resulting in trapped heat in the atmosphere which causes warming of the planet (Oktyabrskiy, 2016). For plants, this could either be a blessing or a curse. 

 

Plate 2. The world map showing projected daily temperatures in July by 2100, under predicted carbon dioxide levels of 935ppm (Gray, 2015).
Plate 1. The world map showing projected daily temperatures in July by 2100, under predicted carbon dioxide levels of 935ppm (Gray, 2015).

 

The good…

Climate change may be beneficial for plants:

  • Enhanced CO2 can increase the photosynthetic rate of plants, which could balance the effect of temperature increases (Thuiller, 2007).
  • With warmer soils, the decomposition rate of organic matter will increase, allowing plants a higher mineral and nutrient availability.
  • Growing seasons for crops may be extended and we could witness an improved agricultural productivity (Brown et al., 2016).

 

The bad…

However, it would be reckless to keep adding CO2 to the atmosphere. Too much of a good thing can be a bad thing right? Once you increase one substance, plants need to increase the rest too! Plants will be incapable of meeting these new requirements.

Changes in rainfall patterns and temperatures can further exacerbate abiotic stresses such as (Naithani, 2016):

  • Drought
  • Waterlogged soils
  • Saltwater inversion
  • Metal contamination

 

These impacts and more make it hard for plants to thrive, with the overarching impact of stunted growth (Worland, 2015).

Plate 2. The invasive Bromus tectorum, a species of the genum Bromus. It is known as the drooping brome or cheat grass.
Plate 2. The invasive Bromus tectorum, a species of the genum Bromus. It is known as the drooping brome or cheat grass. (Source: www.biology.csusb.edu)

Plus, non-native plant species may cross frontiers as conditions become more suitable, out-competing native plants (Thuiller, 2007; Smith et al., 2016; Walter et al., 2002).

The species of long grass, Bromus tectorum, has risen above native plant species in western North America due to being more suited to changes in the wet seasons (Smith et al., 2000).

The ugly…

The human race is a selfish species, perhaps the only way to kick people into action is to present the fact that no plants means no food. Crops won’t grow, land will become barren and food insecurity will explode (Worland, 2015). Could climate change wipe out homo sapiens as well as the worlds plants?

On a lighter note, the outlook may seem dire, but it is not too late for change. As the UN Secretary General Ban Ki-Moon quite rightly stated we are “the last generation that can end climate change”. We can protect and preserve our plants that will provide security to our future generations. Let’s all stop waiting for someone else to solve our problems, and be the change ourselves.

Word count: 499


 

References:

  • IPCC (2013) Climate change: the physical science basis. Working group contribution to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge, UK and New York, USA.
  • Thuiller, W. (2007) Biodiversity: climate change and the ecologist.Nature,448(7153), pp.550-552.
  • Hansen, J., Sato, M., Ruedy, R., Lo, K., Lea, D.W. and Medina-Elizade, M. (2015) Global temperature change. Proceedings of the National Academy of Sciences, 103(39), pp.14288-14293.
  • Oktyabrskiy, V.P. (2016) A new opinion of the greenhouse effect.St. Petersburg Polytechnical University Journal: Physics and Mathematics,2(2), pp.124-126.
  • Brown, I., Thompson, D., Bardgett, R., Berry, P., Crute, I., Morison, J., Morecroft, M., Pinnegar, J., Reeder, T., and Topp, K. (2016) UK Climate Change Risk Assessment Evidence Report: Chapter 3, Natural Environment and Natural Assets. Report prepared for the Adaptation Sub-Committee of the Committee on Climate Change, London.
  • Gray, R. (2015) Our scorched Earth in 2100: Nasa maps reveal how climate change will cause temperatures to soar. [online] Available at: http://www.dailymail.co.uk/sciencetech/article-3125113/Earth-2100-Nasa-maps-reveal-world-need-adapt-rising-temperatures-caused-climate-change.html [Accessed 20 March 2017].
  • Naithani, S. (2016) Plants and global climate change: A need for sustainable agriculture. Current Plant Biology,6(2), p.1.
  • Worland, J. (2015) The weird effect climate change will have on plant growth. [Blog]Time. Available at: http://time.com/3916200/climate-change-plant-growth/ [Accessed 6 Mar. 2017].
  • Smith, S.D., Huxman, T.E., Zitzer, S.F., Charlet, T.N., Housman, D.C., Coleman, J.S., Fenstermaker, L.K., Seemann, J.R. and Nowak, R.S., (2000) Elevated CO2 increases productivity and invasive species success in an arid ecosystem.Nature,408(6808), pp.79-82.
  • Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J., Fromentin, J.M., Hoegh-Guldberg, O. and Bairlein, F., (2002) Ecological responses to recent climate change.Nature,416(6879), pp.389-395.

 

Read more:

http://journal.frontiersin.org/article/10.3389/fpls.2016.01123/full 

http://www.open.edu/openlearncreate/mod/oucontent/view.php?id=22627&printable=1





Will Intensifying Agriculture Save Us, or Starve Us?

The surge in human population in recent years is predicted to reach an unprecedented 9.1 billion people by 2050 – a 14% increase of our current population (McKee et al., 2004). This epidemic of population growth means we are faced with the daunting challenge of attaining sustainable increase in crop production to meet the increasing food demands.

Anthropogenic disturbance in natural landscapes is one of the largest contributors to biodiversity loss. Here is the aftermath of land clearance for palm oil plantations, Borneo. Photo credit: Rhett A. Butler (2012). Available at: https://news.mongabay.com/2012/09/agriculture-causes-80-of-tropical-deforestation/
Anthropogenic disturbance in natural landscapes is one of the largest contributors to biodiversity loss. Here is the aftermath of land clearance for palm oil plantations, Borneo (Butler, 2012).

Global agricultural intensification has increased our food production to meet this demand through conversion of natural to simplified agricultural landscapes and escalating the application of agrochemicals such as pesticides and fertilisers (Matson et al., 1997). This simplification is a major cause of the accelerating loss of biodiversity, which affects ecological processes such as nutrient recycling, carbon storage and pollination (Flynn et al., 2009).

A biotic communities’ functional traits (i.e. characteristics) influences ecosystem functioning through mediating changes in biotic processes, such as predation and competition (Wood et al., 2015). For example, where there are collectively few traits in a community, circumstances of “niche overlap” are common, meaning ability to utilise a broad range of resources within a community decreases, whilst competition for a narrow selection resources increases (Flynn et al., 2009).

Figure 1: Theoretical total functional traits in natural, low-intensity agriculture, intensive agriculture, and managed through polyculture settings4.
Figure 1: Theoretical total functional traits in natural, low-intensity agriculture, intensive agriculture, and managed through polyculture settings (Wood et al., 2015).

Intensive agriculture may degrade (A) the number of functional traits in a given area (functional trait space). However, theoretically implementing adequate management strategies promoting multi-species crops (polycultures) may aid limited recovery of total functional traits (B), recovery to the levels of natural counterparts (C), or even exceed this (D) by endorsing evolution of new species with novel traits (figure 1).

Biodiversity loss through agricultural intensification has been reported for birds, insects, plants and mammals, along with functional trait diversity (Flynn et al., 2009).

 

 

 

Between 1970 and 1990, 86% of farmland bird species had reduced ranges and 83% had declined in abundance [in Europe]” (Benton et al., 2003)

 

The resulting loss of functional traits (including foraging strategies and diet) has significant implications for the removal of insects from farmland, whereby insect subtraction is reduced. The disruptive effects this has on pest communities increases the risk of outbreaks, which not only influences community structures, but hinders crop productivity (Wood et al., 2015).

Application of pesticides to a monoculture crop in an attempt to control pest population. Photo credit Unknown. Available at: http://sitn.hms.harvard.edu/flash/2015/gmos-and-pesticides/
Application of pesticides to a monoculture crop in an attempt to control pest population (Hsaio, 2015)

Shifts toward monoculture (single-species) crops, and reduced predation, facilitates the spread of pests, increasing the risk of epidemics. Pesticides are commonly used as a control measure, although are often toxic to many species.  DDT, commonly used through the mid-20th century, accumulates in increasingly high concentrations up food chains between predators. This concentration may increase thousand-fold or more, of the content in the original source. This caused the endangerment of many predatory birds such as the peregrine falcon and kestrel through thinning their egg shells thus increasing infant mortality. Loss of top predators disrupts regulation of species populations further down the chain, unbalancing the community (Peakall, 1970).

Biodiversity loss is having severe adverse impacts on the health of our biotic communities, and therefore ecosystems. While agriculture cannot be halted all together, we could improve crop strength through diversity through implementing adequate management strategies to promote biodiversity, and use this to control pest outbreaks in an ecologically sensitive manner.

 

References

Benton, T. G., Vickery, J. A. and Wilson, J. D. (2003) ‘Farmland biodiversity: Is habitat heterogeneity the key?’, Trends in Ecology and Evolution, 18(4), pp. 182–188. doi: 10.1016/S0169-5347(03)00011-9.

Butler, R. A. (2012) Agriculture causes 80% of tropical deforestation, Mongabay. Available at: https://news.mongabay.com/2012/09/agriculture-causes-80-of-tropical-deforestation/ (Accessed: 21 March 2017).

Flynn, D. F. B., Gogol-Prokurat, M., Nogeire, T., Molinari, N., Richers, B. T., Lin, B. B., Simpson, N., Mayfield, M. M. and DeClerck, F. (2009) ‘Loss of functional diversity under land use intensification across multiple taxa’, Ecology Letters, 12(1), pp. 22–33. doi: 10.1111/j.1461-0248.2008.01255.x.

Hsaio, J. (2015) GMOs and Pesticides: Helpful or Harmful?, Harvard University: The Graduate School of Arts and Sciences. Available at: http://sitn.hms.harvard.edu/flash/2015/gmos-and-pesticides/ (Accessed: 20 March 2017).

Matson, P. A., Parton, W. J., Power, A. G. and Swift, M. J. (1997) ‘Agricultural Intensification and Ecosystem Properties.’, Science, 277(5325), pp. 504–509. doi: 10.1126/science.277.5325.504.

McKee, J. K., Sciulli, P. W., Fooce, C. D. and Waite, T. A. (2004) ‘Forecasting global biodiversity threats associated with human population growth’, Biological Conservation, 115(1), pp. 161–164. doi: 10.1016/S0006-3207(03)00099-5.

Peakall, D. B. (1970) ‘Pesticides and the reproduction of birds.’, Scientific American, 222, pp. 72–78. Available at: http://sitn.hms.harvard.edu/flash/2015/gmos-and-pesticides/.

Wood, S. A., Karp, D. S., DeClerck, F., Kremen, C., Naeem, S. and Palm, C. A. (2015) ‘Functional traits in agriculture: Agrobiodiversity and ecosystem services’, Trends in Ecology and Evolution. Elsevier Ltd, 30(9), pp. 531–539. doi: 10.1016/j.tree.2015.06.013.

 

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Invasion of the Arctic: How warming temperatures have led to non-native species introduction

Source: Animal Club (2017) Available from: http://elelur.com/mammals/arctic-fox.html
Arctic Fox (Animal Club, 2017.  Available from: http://elelur.com/mammals/arctic-fox.html)

In the eyes of an arctic fox (Alopex lagopus), the temperatures of the tundra provide seamless living conditions. Their adaptations to low temperatures make their arctic habitats suitable for them to hunt, reproduce and in turn survive. However, their survival is threatened by increasing temperatures in the arctic, as it has become more suitable for red foxes (Vulpes Vulpes), too (Killengreen et al., 2007). As the red fox invades the territory of the arctic fox, they undergo competition for land and prey. Although this has not led to a direct decline in arctic fox numbers, it can have further impacts on food webs and community dynamics within the Arctic ecosystem (Gallant et al., 2012).

This is just an example of the new reality in the Arctic; ice is melting due to increased temperatures, and the ecosystem is changing vastly (Serreze et al., 2000). Many of us are aware that global temperatures are rising due to increased greenhouse gas emissions entering the atmosphere, however the rate of temperature change varies across the globe. Where average temperatures have increased by 0.4°C over the past 150 years, it is believed that warming in arctic regions has been almost 3 times higher (IPCC, 2014).

The increased warming creates an environment which is suitable for other, non-native species (Post et al., 2009) – such as the example of the Red Fox. Species towards the South of the Arctic have increased their range, placing pressure on the existing Arctic communities (Root et al., 2003). This ‘invasion’ is not limited to animal species; invasive species in the form of plant communities can also intrude on the ecosystem. For example, the warming has allowed shrub tundra to expand into a wider variety of habitats, and Boreal forest has begun to infringe on the tundra ecosystem (Hinzman et al., 2005).

Source: Animal Photgraphics (2017) Available from: http://alaskaphotographics.photoshelter.com/image/I00009qTaSPpYpaA
Arctic Ground Squirrel. (Animal Photgraphics, 2017. Available from: http://alaskaphotographics.photoshelter.com/image/I00009qTaSPpYpaA)

Another example is of the arctic ground squirrel (Urocitellus parryii), which acts as an ecosystem engineer through its key role in the food web (Wheeler, 2011). The arctic ground squirrel burrows into vegetated land as a mechanism for survival. The burrowing action also changes the composition of the soil, which is important for other ecological processes. However, as boreal, woody forests become more prominent than the easily accessible vegetation, the arctic ground squirrel loses its habitat (Donker & Krebs, 2011).

 

 

 

Figure 1. Predicted global surface temperature change, based on carbon emissions scenarios (IPCC, 2013).
Figure 1. Predicted global surface temperature change, based on carbon emissions scenarios (IPCC, 2013).

The Arctic ecosystem is so complex that the full effects of climate change are not yet understood. This means that the invasive species described above have the potential to interrupt even more ecological processes and food webs. This could also affect human livelihood as we also rely on the stability of the food chain for survival. Furthermore, global warming is expected to cause temperatures to increase even more, dependent on emissions scenarios (Figure 1). This would cause the number of invasive species in both terrestrial and marine ecosystems to increase, threatening the existing communities to an even greater extent.

 

 

References

Donker, S. A., Krebs, C. J. (2011) Habitat Specific Distribution and Abundance of Arctic Ground Squirrels (Urocitellus parryii) in Southwest Yukon. Canadian Journal of Zoology, 89, 570-576.

Gallant, D., Slough, B. G., Reid, D. G., Berteaux, D. (2012) Arctic fox versus red fox in the warming Arctic: four decades of den surveys in north Yukon. Polar Biology, 35(9), 1421-1431.

Hinzman, L. D., Bettez, N. D., Bolton, W. R. et al. (2005) Evidence and Implications of Recent Climate Change in Northern Alaska and Other Arctic Regions. Climatic Change, 72(3), 251-298.

IPCC (2013) Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA, 1535 pp.

IPCC (2014) Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland, 151 pp.

Killengreen, S. T., Ims, R. A., Yoccoz, N. G., Brathen, K. A., Henden, J., Schott, T. (2007) Structural Characteristics of a Low Arctic Tundra Ecosystem and the Retreat of the Arctic Fox. Biological Conservation, 135(4), 459-472.

Post, E., Forchhammer, M. C., Bret-Harte, S. M. et al. (2009) Ecological Dynamics Across the Arctic Associated with Recent Climate Change. Science, 325(5946), 1355-1358.

Root, T. L., Price, J. T., Hall, K. R., Schneider, S. H., Rosenzweig, C., Pounds, J. A. (2003) Fingerprints of Global Warming on Wild Animals and Plants. Nature, 421, 57-60.

Serreze, M. C., Walsh, J. E., Chapin, F. S., III, Osterkamp, T., Dyurgerov, M., Romanovsky, V., Oechel. W. C., Morison, J., Zhang, T., Barry, R. G. (2000) Observational Evidence of Recent Change in the Northern High Latitude Environment. Climate Change, 46, 159-207.

Wheeler, H. C. (2011) Arctic Ground Squirrels Urocitellus parryii as Drivers and Indicators of Change in Northern Ecosystems. Mammal Review, 43, 238-255.

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Plants Revealed to be More Efficient at Higher CO2 Levels

As we enjoy a varied diet of carbohydrates, proteins and fats, for plants it is the gas carbon dioxide (CO2), water and sunlight (figure. 1).

Figure. 1 Pedunculate Oak Tree; a temperate plant species that could be impacted by changing atmospheric conditions.
Figure. 1 Pedunculate Oak Tree in sunlight (Lind).

It is not just CO2 use which is made more efficient at elevated CO2 levels, water efficiency is greater as less water is lost from leaf pores; stomata. FACE (Free-Air CO2 Enrichment) experiments with soybean show that leaf pore conductance is not adapted to elevated CO2 but rather maintain decreased conductance. Furthermore, this increase in water efficiency is consistent between the leaf and canopy levels (Leakey et al, 2009).

 

It was also thought that higher CO2 levels lead to increased efficiency of nitrogen, a mineral required for growth, as plants grown at these levels do not have as much nitrogen present. These high CO2 grown plants also have a greater biological mass than those grown at normal CO2 conditions. However these CO2 levels where not found to affect levels of biological mass attained over plant lifetime which indicates that an accelerated period of growth that used up nitrogen reserves (Coleman et al, 1993). Increased CO2 levels are thought to contribute to increased uptake of nitrogen by plant roots rather than increased plant efficiency regarding nitrogen. Further FACE experiments at three separate forest locations showed that increased biological mass corresponded to increased nitrogen uptake from the soil. However this is limited to areas where nitrogen soil supply exceeds demand and is therefore unlikely to be seen in all plants worldwide (Finzi et al, 2007).

 

These FACE experiments are advantageous as they allow CO2 to be applied to a specific area of a wide range of ecosystems from desert to tropical forest. Trees as tall as 25m can be used in these experimental plots which can be as large as 30m in dimeter (Norby and Zak, 2011).

 

Figure.1 Atmospheric carbon dioxide (CO2) levels from 1950-2010 (IPCC, 2013)
Figure.2 Atmospheric carbon dioxide (CO2) levels from 1950-2010 (IPCC, 2013)

Scientists have been documenting rising atmospheric CO2, which is associated with planetary warming, for almost 70 years now, since 1950 (figure. 2). It is widely accepted that this change in CO2 has arisen from human industrialisation. While it seems that plants can positively cope with this change this conclusion must not be taken at face value and further studies must be undertaken.

 

 

 

  • Coleman, J.S., McConnaughay, K. D. M and Bazzaz, F. A. (1993). Elevated CO2 and Plant Nitrogen-Use: is reduced Tissue Nitrogen Concentration Size Dependent?. Oecologia. 93, 195-200.
  • Drake, B. G., Gonzalez-Meler, M. A and Long, S. P. (1997). More Efficient Plants: a Consequence of Rising Atmospheric CO2. Ann. Rev. Plant. Physiol. 48, 609-639.
  • Finzi, A. C., Norby, R. J., Calfapietra, C., Gallet-Budynek, A., Gielen, B., Holmes, W. E., Hoosbeek, M. R., Iversen, C. M, Jackson, R. B., Kubiske, M. E, Ledford, J., Liberloo, M., Oren, R., Polle, A., Pritchard, S., Zak, D. R., Schlesinger, W. H and Ceulemans, R. (2007). Increased in Nitrogen Uptake rather than Nitrogen-Use Efficiency support higher rates of Temperate Productivity under Elevated CO2. PNAS. 104 (35), 14014-14019.
  • IPCC, 2013: Summary for Policymakers. In: Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change [Stocker, T.F., D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex and P.M. Midgley (eds.)]. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA.
  • Leakey, A. D. B., Ainsworth, E. A., Bernacchi, C. J., Rogers, A., Long, S.P and Ort, D. R. (2009). Elevated CO2 Effects on Plant Carbon, Nitrogen and Water Relations: six important lessions from FACE. Journal of Experimental Botany. 60 (10), 2859-2876.
  • Lind, J. © Photo of Pedunculate Oak Tree. Available: http://www.arkive.org/pedunculate-oak/quercus-robur/image-A20783.html. Last accessed 20th March 2017.
  • Norby, R. J and Zak, D. R. (2011). Ecological Lessons from Free-Air CO2 Enrichment (FACE) Experiments. Annual Review of Ecology, Evolution and Systematics. 42. 181-203.

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Plants are losing their jobs… FAST!

Figure 1: Destruction of plant habitat from palm oil production.
Figure 1: Destruction of plant habitat from palm oil production.

So, the boss tells you the company’s going through a bit of a shake-up due to the current market conditions and needs a ‘more efficient’ workforce. He apologetically explains that you and Tim down the hall… are doing a one-person job. Plant extinctions might be happening in much the same way… for the moment.

 

The rate of extinction is too damn high, and it’s driven primarily by human activities creating habitat loss, introduced exotic species and global warming. Using even the most conservative estimates, it’s thought we’re currently experiencing the 6th mass extinction in Earth’s history1. Previous events include the one that took out the dinosaurs. It’s estimated that we’re losing species at 1000-10000 times the background rate (extinction rate if humans weren’t around)2. For plants specifically, 21% of species are considered threatened with extinction according to ICUN red list criteria3 and less species equals less diversity.

 

But does losing biodiversity in ecosystems matter? Can the same amount of just one species not be as successful? One of the first studies to test this was performed in the Ecotron4,5, sadly not a planet saving robot, but a laboratory with completely controllable sealed environments. Simply put, they found an increase in mean biomass (functioning) with increasing diversity. Similarly scientists running an unrelated 11 year grassland experiment in Minnesota realised that their squares of grass maintained at different levels of diversity would be perfect for investigating this question6,7. They also found higher productivity with increased plant diversity and further encountered increased stability of the ecosystem in response to drought. But these experiments took place in one location, can this be repeated across the world? The Biodepth Project8 did just that, monitoring controlled grasslands in eight different European countries. Once again, increased productivity with greater diversity was observed overall. So, these microcosm experiments seem to be telling us that if we lose diversity through extinction it will have a negative effect on the functioning of whole ecosystems.

 

Figure 1: A diagram showing the predominant curves found when plotting a measure of ecosystem functioning (y-axis) against species diversity (x-axis).
Figure 2: A diagram showing the predominant curves found when plotting a measure of ecosystem functioning (y-axis) against species diversity (x-axis).

 

Where does redundancy fit into this? Take a look at Figure 2. The straight line running through the middle of A, B and C depicts a situation where every species makes a unique contribution; you’re better with IT, Tim down the hall is better with report writing. However, what’s found in the majority of research9 is the saturated curve at the top of each graph. Here we see an initially slow decline in functioning as most species that die off have one doing something similar to take its place; you and Tim basically do the same job. This is called species redundancy. But once we run out of non-unique species, we suddenly spiral into a fast and dramatic decline in functioning.

 

What’s worrisome about this? We are currently not sure where exactly on this saturated curve most of our ecosystems sit. Can we rely on species redundancy for a long time to come or are we at the edge of the precipice about to destroy the productivity of the natural world. I’d rather not find out.

 

 

References:

  1. Ceballos, G., Ehrlich, P.R., Barnosky, A.D., García, A., Pringle, R.M. and Palmer, T.M. 2015, ‘Accelerated modern human–induced species losses: Entering the sixth mass extinction’, Science Advances, 1 (5): e1400253.
  2. Chivian, E. and Bernstein, A. (eds), 2008, Sustaining life: how human health depends on biodiversity. Oxford University Press, Oxford.
  3. Kew, R.B.G. 2016, The state of the world’s plants report–2016, Kew: Royal Botanic Gardens.
  4. Naeem, S., Thompson, L.J., Lawler, S.P., Lawton, J.H. and Woodfin, R.M. 1995, ‘Empirical evidence that declining species diversity may alter the performance of terrestrial ecosystems’, Philosophical Transactions of the Royal Society of London B: Biological Sciences, 347 (1321): 249-262.
  5. Naeem, S., Thompson, L.J., Lawler, S.P., Lawton, J.H. and Woodfin, R.M. 1994, ‘Declining biodiversity can alter the performance of ecosystems’, Nature, 368 (6473): 734-737.
  6. Tilman, D. and Downing, J.A. 1994, ‘Biodiversity and sustainability in grasslands’, Nature, 367 (6461): 363-365.
  7. Tilman, D., Wedin, D. and Knops, J. 1996, ‘Productivity and sustainability influenced by biodiversity in grassland ecosystems’, Nature, 379 (6567): 718-720.
  8. Minns, A., Finn, J., Hector, A., Caldeira, M., Joshi, J., Palmborg, C., Schmid, B., Scherer-Lorenzen, M., Spehn, E. and Troumbis, A. 2001, ‘The functioning of European grassland ecosystems: potential benefits of biodiversity to agriculture’ Outlook on Agriculture, 30 (3): 179-185.
  9. Cardinale, B.J., Matulich, K.L., Hooper, D.U., Byrnes, J.E., Duffy, E., Gamfeldt, L., Balvanera, P., O’Connor, M.I. and Gonzalez, A. 2011, ‘The functional role of producer diversity in ecosystems’, American journal of botany, 98 (3): 572-592.




Plant adaption to changing climate through studying global scale response experiments – FACE (Free Air Carbon dioxide Enrichment)

Jade Lemm

 

For the last 400,000 years plants have been adapted to low Carbon dioxide (CO2) of approximately 180ppm (parts per million) up until the Anthropocene era. However low CO2 was not always the case, up until the end of the Phanerozoic era concentrations were suggested to be minimal of 100 times higher current Anthropocene era CO2 (Kasting, 1987). In this current era CO2 has been seen to be rising at an ‘unprecedented rate’ from 1750 of 31% from sources natural and anthropogenic but the dramatic increase can be detected firstly from the industrial revolution (Steffen et al, 2015). These green plants such as forests are part of terrestrial sinks taking up 120 GTC (Giga Tonnes Carbon) per year dependant on location and time of year (Hartmann, Tank & Rusticucci, 2013). The time of year is important as an annual flux in CO2 is indicated by figure 1 showing the change in vegetative seasonality. Plants photosynthesize and draw the CO2 down in the summer but in the winter plants die back causing high CO2 concentrations shown by figure 2 (Gore, 2006).

 

co2-flux

Fig 1. – The increase of CO2 over time showing the displacement of seasons (Gore, 2006).

seasonal-co2-flux

Fig 2. – Change in CO2 over the seasons due to plant photosynthesis (Gore, 2006).

 

It has been debated on a global scale of how terrestrial and marine species would adapt to the rate of CO2 increase as it indicates to be a similar outcome to the Phanerozoic era. For the terrestrial green plant species past data over the 1900’s show that plants were adapted to higher CO2 makes higher plant respiration rates (Wullschleger, Ziska & Bunce, 1994). To adapt to these levels of high CO2 green plants use an enzyme called ‘Rubisco’ but is not an efficient plant as it slows water and nutrients. However, genetic engineering methods are still looking into enhancing this for global future food crisis as 50% demand increase is predicted (Whitney, Houtz & Alonso, 2011). The only way to confirm whether terrestrial plants can adapt to global changing CO2 is to study the effects in controlled environments such as Free Air Carbon dioxide Enrichment (FACE). FACE provides global scale responses from open air natural conditions with releasing controlled CO2 from pipes relying on wind to disperse it. This enables the study of modelling for future CO2, the increase of CO2 under these conditions have provided different effects on different species (McLeod & Long, 1999). For example, seeds of rice provided a yield growth increase of 5-7% under conditions of 550ppm for future conditions, compared to wheat at the same future conditions showed an increase of 27% with a further increase of 3% up to 650pmm (Ainsworth & Long, 2005). But these experiments all depend on the environment that they are placed in as it is all achieved by natural dispersal and planting time, the plants were only successful if early planting was achieved with the correct temperature and moisture. This varied at locations so studies in Australia would have to monitor the crops more carefully compared to Arizona (Mollah, Norton & Huzzey, 2009). However, more research is needed in this still unknown area to quantify the future.

 

References

Ainsworth, E.A. and Long, S.P., 2005. What have we learned from 15 years of free‐air CO2 enrichment (FACE)? A meta‐analytic review of the responses of photosynthesis, canopy properties and plant production to rising CO2. New Phytologist, 165(2), pp.351-372.

Gore, A., 2006. An inconvenient truth: The planetary emergency of global warming and what we can do about it. Rodale.

Hartmann, D.L., Tank, A.M.G.K. and Rusticucci, M., 2013. IPCC fifth assessment report, climate change 2013: The physical science basis. IPCC AR5, pp.31-39.

Kasting, J.F., 1987. Theoretical constraints on oxygen and carbon dioxide concentrations in the Precambrian atmosphere. Precambrian research, 34(3-4), pp.205-229.

McLeod, A.R. and Long, S.P., 1999. Free-air carbon dioxide enrichment (FACE) in global change research: a review. Advances in ecological research, 28, pp.1-56.

Mollah, M., Norton, R. and Huzzey, J., 2009. Australian grains free-air carbon dioxide enrichment (AGFACE) facility: design and performance. Crop and Pasture Science, 60(8), pp.697-707.

Steffen, W., Broadgate, W., Deutsch, L., Gaffney, O. and Ludwig, C., 2015. The trajectory of the Anthropocene: the great acceleration. The Anthropocene Review, 2(1), pp.81-98.

Whitney, S.M., Houtz, R.L. and Alonso, H., 2011. Advancing our understanding and capacity to engineer nature’s CO2-sequestering enzyme, Rubisco. Plant Physiology, 155(1), pp.27-35.

Wullschleger, S.D., Ziska, L.H. and Bunce, J.A., 1994. Respiratory responses of higher plants to atmospheric CO2 enrichment. Physiologia Plantarum, 90(1), pp.221-229.

 

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