Bob Birrell

Walter Jehne[*]

The nutrition of agricultural soils
Sustaining productive farming systems

Roundtable discussion of this paper

Life on earth over the past 3.8 billion years has substantially relied on photosynthesis, the conversion of sunlight, CO₂ and water into carbohydrates - initially by blue green algae and then plants to sustain itself.

Whereas sunlight, CO₂ and water are generally available, photosynthesis is often limited by the availability of some of the 16 major, minor and trace nutrients essential for plant growth.

Apart from nitrogen, which is sourced from the atmosphere, mineral nutrients have to be obtained from rocks or their weathered derivative, soils. The mineral nutrients must be present but also available for uptake by the plant roots; either via the absorption of soil water or through their selective uptake by symbiotic fungal associations called mycorrhizas.

Soils differ greatly in their level and composition of nutrients and in how those nutrients are held in either rocks, on soil surfaces, on organic matter or as chemical ions in soil solution.

Available nutrients - How nutrients are held fundamentally affects their solubility and hence their availability for uptake by plants and associated symbiotic associates. While soils may contain high levels of nutrients in total, such nutrients may not be soluble or available to the plant, significantly limiting the bio-productivity or fertility of that soil.

Consequently the factors that govern the availability of essential plant nutrients are often more important in governing the fertility of a particular soil than the level of those nutrients. Similarly the effectiveness of nutrient additions via fertilizers may also depend on how much remains available and for how long rather than on the levels that are added. For example many soils with high iron and aluminum oxide levels can occlude over 98% of the soluble phosphate added as fertilizers making it unavailable for uptake and the intended increased plant growth.

Soil microbes - The presence and activity of specific micro-organisms can often become the most important factor in enhancing and sustaining the fertility and productivity of soils. Indeed microbial associations govern most of the nutrition, and hence existence and bio-productivity of most of the world’s natural vegetation, particularly for perennial systems growing on more weathered, lower nutrient status soils.

While the importance of these microbial processes in the availability of nutrients to plants has been known for decades, their significance has not been widely appreciated in agriculture. As such the nutrition and productivity of agricultural plants has often been based on the speedy and opportunistic harvesting of natural or added nutrients as these are made available by periodic burning, soil disturbance or nutrient inputs.

As the availability and affordability of oil based fertilizer inputs decline, food securities will increasingly need to be based on sustainable perennial farming and soil nutrient systems. The understanding and management of the key microbial processes governing the fixation, solubility, availability, uptake and recycling of essential plant nutrients will become fundamentally important to sustaining agricultural productivities and food securities in this new global environment.

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The nutrition of agricultural soils

Whereas humans have evolved over the past million years as hunters and gatherers utilizing foods produced from such natural perennial bio-systems and nutrient processes, agriculture over the past 10,000 years but particularly industrial farming systems over the past 100 years have been based on fundamentally different nutrient strategies that have different impacts.

Rather than managing and harvesting food from broadacre perennial systems, intensive agriculture has concentrated and survived in particular unique locations where there were either highly fertile nutrient rich soils or where natural processes resulted in the regular addition and replenishment of essential nutrients. As a result most of the world’s agriculture has been, and still is concentrated on:

• The high nutrient soils formed as a result of recent glaciations, as for example in Europe, Russia and North America,

• On soils with previous or intermittent volcanic nutrient additions as in the case of Java, Darling Downs, Japan or,

• On river sediments such as in Egypt, Iraq, India, China in which nutrients are periodically replenished via the deposition of fresh nutrient rich sediments.

Such soil and nutritional resources have been fundamental to each of the world’s civilizations. Where natural processes have sustained soil fertilities such as in the Nile or where soils were managed to sustain and enhance nutrient cycling, as in China, civilizations have survived. However in most instances former civilizations, such as Babylon, Lebanon, Crete, Greece, Rome, Carthage, the Maya, Easter Island and others, have each failed directly because of their inability to sustain their original fertile soils and with that their essential food requirements.

Modern agriculture - Over the past 150 years ‘scientific agriculture’ has made it possible to grow crops even on soils of lower natural fertility via the addition of nutrients in fertilizers. This has enabled global populations to increase from some one billion to the present 6.5 billions over that period. However, the productivity of these crops and the viability of their dependent societies is now often highly dependent on the continued input of such fertilizers and their impacts on the soil.

The long term dependence on fertilizer additions raises sustainability challenges including:

• The finite limits and cost of accessing mineral deposits for conversion into fertilizer.
• The energy cost involved in the mining, transport, processing, distribution, and application of these fertilizers relative to the energy returns from the crops produced. As the oil used in these fertilizer processes becomes more expensive the returns from many current agricultural systems may no longer be economically viable.
• The serious degradation in the organic matter status and structure of many farmed soils as a result of inappropriate fertilizer use. This degradation, by decreasing water infiltration, availability, root proliferation and increasing toxic and saline effects can limit plant growth resulting in decreased fertilizer effectiveness as well as increased requirements to sustain former yields.
• The often rapid fixation of much of the added fertilizer nutrients onto soil surfaces so that they are unavailable for plant uptake and growth, or the leaching of more soluble fertilizer nutrients from soils into streams to create pollution risks.
• Nutrient deficiencies and toxicities as a result of nutrient in-balances due to inappropriate fertilizer additions. Healthy soils and plants generally require a balanced availability of all essential macro and micro nutrients with the overall growth response often being governed by the availability of the most limiting nutrient which may be affected by excesses of other added nutrients.
• The effect of inappropriate fertilizer additions on both the nutritional balance and value of the resultant crops and foods as well as the effect of fertilizers in altering the susceptibility of some crops to disease and stress factors.

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Processes for sustaining highly productive but low nutrient input farming

Although the above reinforce our dependency on and potential consequences of our common high nutrient input agricultural systems, as the availability and affordability of oil declines we will need to develop more sustainable and productive agro-ecosystems that are less dependent on repeated expensive high nutrient inputs and the degradation of natural soil capital.

Although such systems have existed and supported sustainable communities for millennia, often in remote tribal cultures and via shifting cultivation systems such as in Papua New Guinea and the Amazon, such traditional systems could not support the current global population. However an understanding of the nutrient dynamics in such agricultural systems may be critical in restoring the nutrition and bio-productivity of future low input farming systems.

Studies of the nutrient dynamics in such forests and in their periodic clearing, burning and use for shifting cultivation cropping confirms that natural bio-systems, far from being dependent on fertile high nutrient soils, have evolved means of sustainably supporting highly bio-productive and diverse systems even on extremely low nutrient soils. Rather than depending on high nutrient levels or inputs, as in our current farming systems, these natural productive bio-systems have evolved extremely efficient nutrient cycling systems. This enables adequate essential nutrients to be made available optimally where and when required for plant growth, despite the quantity of nutrients within that system often being extremely low.

As a result some of the world’s most bio-productive natural ecosystems occur on some of the world’s lowest nutrient status soils; such as the subtropical rainforests growing on silicaeous sand dunes at Cooloola and Fraser Island in Australia or the rainforests growing on low nutrient oxisols and latesols throughout the Amazon.

Microbial recycling - The very rapid and efficient cycling of the very limited quantities of essential nutrients is made possible through a range of soil micro-organisms, specifically mycorrhizal fungi. These fungi are directly involved in the bio-degradation of litter, the solubilization and efficient uptake of key nutrients from organic and mineral surfaces and their translocation to the actively growing plant tissues. Studies with radioactive labeled nutrients confirm that such microbial symbioses can recycle nutrients from fresh litter back into the plant within minutes, rather than the weeks or even years required for nutrients to recycle via chemical processes.

As it is possible to enhance and manage these microbial recycling systems, the potential exists to develop similar highly efficient nutrient cycling strategies in highly productive food and biomass producing agro-ecosystems even on low nutrient soils without high fertilizer inputs.

Provided that only 'stored solar energy' as biomass or sugars is used and no nutrients are quarried and exported from the site it should be possible for such bio-systems to be sustained at high levels of productivity and profitability. Similarly, provided any nutrients that are removed in the foods produced are returned to the site as recycled wastes, it should be possible to enhance and sustain the bio-productivity of such systems for many future food and energy crops.

Research has confirmed that it is practical and feasible to select, introduce and enhance the activity of highly efficient microbial symbioses to optimize the nutrition and sustained productivity of different agro-ecosystems. Field and glasshouse inoculation studies confirm that such symbioses can greatly enhance the nutrition and growth of crop plants in unfertilized soils similar to those with optimal fertilizer additions. Although establishing such optimal symbioses and nutrient cycling systems involves more than just 'adding microbes', the fact that selected symbioses can be as effective as fertilizers in stimulating crop growth - while also being free, natural and sustainable - reinforces their significance for low input food systems.

Major opportunities exist to design highly productive low input agro-ecosystems based on these natural nutritional cycles and meet our food security imperative in a post cheap oil economy.

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Keith Boardman

Contents
Part 1: Photosynthesis, energy and food chains

Part 2: The process of photosynthesis in more detail

References
Glossary

Part 1 Photosynthesis, energy and food chains

Photosynthesis is the process by which plants and algae use energy from sunlight to synthesize carbohydrates from carbon dioxide and water. All plants and animals as well as most microbes are dependent on the products of photosynthesis for their existence.

Photosynthesis is represented by the reaction:

carbon dioxide + water = carbohydrate + oxygen

CO2 + H2O = CH2O + O2

Photosynthesis takes place in very small particles in the plant cells called chloroplasts. The process consists of two distinct phases: a light phase and a dark phase.

In the light phase sunlight is absorbed by chlorophyll and converted into chemical energy and results in the formation of two energy carrier molecules which play an essential role in the dark phase. They are nicotinamide adenine dinucleotide phosphate (NADPH) and adenosine triphosphate (ATP).

Thus, the energy requirement of the reaction (480 kilojoules per mole of CO2) is provided by sunlight.

In the second, dark phase NADPH and ATP provide the energy which is used for the synthesis of carbohydrate. Chlorophyll is not involved in this phase.

Energy flow in ecosystems

Energy rich solar radiation that would otherwise be transformed to low energy heat is diverted into the ‘steam of life’ by the process of photosynthesis. Energy flows through ecosystems from the green plants and algae, called autotrophs or producer organisms to herbivores, the primary consumers that use the autotrophs as their food source and then to carnivores, secondary consumers, as they eat the herbivores. Some organisms such as humans are omnivores, eating both plant products and animal products.

There is loss of energy and biomass as the energy passes from one organism to another. The energy stored in carbohydrate and other organic material consumed as food by an organism is used in respiration for growth or maintenance with the release of some low-grade heat to the environment. Organic matter is lost as excretory material or upon the death of an organism when there is decomposition by microorganisms, the decomposers of the ecosystem. Energy does not recycle and ultimately the fate of energy in the ecosystems is to be lost as heat. The flow of energy in an ecosystem is often portrayed as a food chain or food web.

Compared with trees and many other terrestrial plants, the autotrophs of the ocean, the phytoplankton, contain a very small amount of the total biomass of the ocean food chain because they are rapidly consumed by predators.

Primary production

Trees and other terrestrial forms of vegetation with large surface areas of leaves are well designed for the collection of solar energy. About 45% of sunlight is at wavelengths that are absorbed by the photosynthetic pigments and under ideal greenhouse conditions about 9-10% of the solar radiation is fixed in carbohydrates and other plant organic compounds. Nearly 50% of the fixed carbon is lost by dark respiration at night and by photorespiration. The net maximum efficiency of photosynthesis under these ideal conditions is 5%-6 %, equivalent to a net primary production (NPP) of 5-6 x 10¹² tonne of dry organic material.

A peak efficiency of solar energy conversion of 4.5% has been measured for sugar beet (a C3 plant) and maize (a C4 plant - see Part 2 below) grown for short periods in the field under optimal conditions. However, maximum growth rates of high yielding crops averaged over the usual period of growth represent an efficiency of solar energy conversion of 1%-2%. On a global scale, terrestrial photosynthesis is severely limited by availability of water and nutrients or by low temperature. Marine photosynthesis is limited by ocean nutrients. The oceans, in general, have very low levels of some of the minerals needed for plant growth, since the mineral-rich waters sink to the bottom of the ocean. Only where deep water currents rise as upwellings to the surface or where major rivers disgorge their contents into neighbouring seas do the vital nutrients reach a level sufficient to allow for high marine primary production. A satellite-based study of marine phytoplankton showed a decrease in global production of phytoplankton in years of higher ocean surface temperature. The reduction is attributed to a reduction in upwelling. Net primary production (NPP) overall in the marine environment is slightly less than NPP in the terrestrial environment.

The average photosynthetic efficiency on a global scale is approximately 0.2 %. This is equivalent to an annual global NPP of 250 petagram (Pg) of organic material or 250 x 10⁹ tonne.

Food chain

A food chain indicates the flow of energy from the producer autotrophs through the series of consumer organisms that feed on each other. Only a fraction of the energy in plants and algae is transferred to herbivores and only a fraction of the energy in herbivores is transferred to carnivores. As a rough estimate approximately ten percent of the biomass of one trophic level is transferred to the next higher trophic level. In agricultural systems there are large inputs of fertiliser and large outputs as agricultural produce is harvested. In terms of energy, agricultural systems increase the efficiency of solar energy conversion and increase the NPP for human consumption.

Appropriation of Net Primary Production (NPP) by humans

The fraction of the Earth’s NPP appropriated by humans is a measure of human impact on the biosphere.

In 1986, Vitousek et al. published estimates of the fraction of NPP appropriated by humans. Their estimates were the outcome of an extensive analysis of the data of many previous studies of land use and NPP. In their paper they provide three calculations of the human appropriation of NPP; a low calculation, an intermediate one and a high one.

The low calculation was simply the amount of organic material consumed by humans.

Assuming an average calorific intake of 2500 kcal/person/day and a world population of 5 billion, the annual consumption of organic material by humans was calculated as 0.91 Pg. Plant products accounted for 0.76 Pg and animal products 0.15 Pg. The amount of agricultural plant products harvested for human consumption was 1.15 Pg indicating a loss of 0.39 Pg or 34% to pests or post-harvest spoilage. An estimate of consumption of plant products by livestock was equivalent to 2.2 Pg of dry organic material. This indicated an efficiency of 6.8% for conversion of plant material to human food. Total annual fish catch was 0.02 Pg. Although the consumption of fish by humans is a very small fraction of marine NPP some fisheries are under threat due to overfishing. It was estimated that humans use 2.2 Pg of wood (dry weight) from forests. In developed countries most of the wood is used for construction and as fibre for paper manufacture, whereas in developing countries firewood is the principle use.

Vitousek et al. estimated that humans use approximately 7.2Pg of organic material each year or about 3% of the annual global NPP.

For their intermediate calculation Vitousek et al. included the NPP of the Earth’s croplands, estimated as 15 Pg/yr and the NPP of land that had been converted during human history to human-controlled pastures and forest plantations. The NPP of the derived grazing land (9.8 Pg/yr) was estimated from the average productivity of the converted woodlands and grasslands. Plantation forests were estimated to add 1.6 Pg/yr to the NPP appropriated by humans. Yitousek et al. considered that all cropland NPP, derived grazing land NPP and plantation forest NPP was unavailable to the natural community and therefore co-opted by humans. The NPP consumed by livestock on natural grazing land (0.8Pg/yr) also represents NPP appropriated by humans. Fires caused by humans on natural grazing lands consume biomass estimated as 1.0 Pg/yr. The waste from the harvesting of forests for construction and fibre was estimated as 1.3 Pg/yr. A significant component of the intermediate calculation was the biomass (8.5 Pg/yr) that is destroyed by the clearing of forests, either for shifting cultivation or permanent forest clearing. Land under cities and highways represents an appropriation of 2.6 Pg of NPP.

From these calculations Yitousek ei al. estimated that humans co-opt 42.6 Pg of NPP each year, equivalent to approximately 19% of global NPP or 31% of terrestrial NPP.

The high calculation included both the NPP co-opted by humans and an estimate of the potential NPP that is lost as a consequence of the presence of humans on Earth. The high calculation suggests that humans appropriate nearly 40% of potential terrestrial NPP or 25% of global NPP.

The calculations of Vitousek et al. were based on data from small field studies made prior to 1986. In 2001, Rojstaczer el al. calculated human appropriation of the NPP from contemporary data, many of which were satellite based and collected at global and continental scales. Their mean estimate showed that humans appropriate 39 Pg/yr of organic material or 32% of their estimate of terrestrial NPP. This agrees remarkably well with the intermediate calculation of Vitousek et al.

Ecology of photosynthesis in sun and shade

Plants growing under a very low light intensity on the floor of a dense rain forest synthesise more antenna chlorophyll to improve the capture of available light quanta. They have less Rubisco (an essential enzyme involved in the synthesis of carbohydrate – see Part 2 below) than plants growing at high light intensity. Many plants have the ability to change their photosynthetic capacity (termed acclimation) depending on the light intensity under which they are growing. At high light intensity the plant invests more of its synthetic capacity to increase the amounts of Rubisco and the photosynthetic electron carriers in proportion to the amount of chlorophyll. The leaf morphology can change with an increase in the frequency of stomates for improved uptake of atmospheric CO2. Plant species, however, differ markedly in the acclimation of their photosynthetic response to light intensity. Marine phytoplanton also have the ability to acclimate to light intensity.

Plants grown under high CO2 concentrations show higher growth rates (termed CO2 fertilisation). The increasing atmospheric concentration of CO2 due to fossil fuel burning should have a beneficial effect on plant growth but the long term consequences of increased CO2, coupled to rising temperatures on ecological plant communities are unknown. It is possible that some species of plants will acclimate to long term growth in high CO2 by reducing the amount of Rubisco and the rate of plant growth.

Environmental factors such as temperature, light intensity, CO2 concentration and water and nutrient availability will affect the photosynthetic process differently in different species to the advantage of some and the disadvantage of others with impacts on the ecology of plant communities.

Part 2: The process of photosynthesis in more detail

Light phase

Higher plants and green algae contain two green pigments, chlorophyll a and chlorophyll b and yellow pigments, the carotenoids. The red and blue-green algae do not have chlorophyll b but they contain red and blue pigments called phycobilins.

The secret of the conversion of light energy to chemical energy in photosynthesis lies in the way the chlorophyll molecules are combined with proteins within small structures in the plant cell called chloroplasts.

Light and electron microscopy of higher plants show chloroplasts as saucer shaped bodies 5 to 10 um in diameter. Each chloroplast has an outer membrane or envelope and internally it contains a system of flattened membranes (thylakoids) arranged in stacks, known as grana. The grana are interconnected by a system of loosely arranged thylakoids. The chlorophyll molecules and the other components of the light phase of photosynthesis are combined with proteins within the thylakoid membranes.

Most of the chlorophyll a molecules as well as all of the chlorophyll b and the carotenoids are not involved directly in the photochemical reaction where light energy is converted to chemical energy. They function as an ‘antenna’ of light-harvesting pigments to absorb light quanta and transfer the energy to special chlorophyll a molecules where the light energy is converted to chemical energy. These light-harvesting chlorophylls are organised into units of about 200 molecules. Each unit, known as a photosynthetic unit, has one reaction centre chlorophyll a molecule which, on excitation, promotes an electron transfer and charge separation.

Two photosystems

The light phase of photosynthesis requires the cooperation of two different chlorophyll assemblies and photochemical reactions, known as photosystem 1 (PS-1) and photosystem 2 (PS-2).

Photosystem 2 catalyses the photochemical splitting of water and the evolution of molecular oxygen to the atmosphere. Recent structure studies by Xray crystallography have illustrated a very complex structure for the organisation of the chlorophyll molecules and proteins in PS-2. The site for water splitting involves a cluster of four manganese ions and a calcium ion surrounded by the side chains of proteins. The details of the chemistry of the manganese cluster in water splitting has not been elucidated although it has been known for 30 years that there is an accumulation of four positive charges on the manganese cluster before a molecule of O2 is produced. Excitation of chlorophyll a in the reaction centre of PS-2 by transfer of energy from the antenna chlorophylls of PS-2 produces a charge separation leading to the oxidation of water and the reduction of a quinone (plastoquinone) within the thyakoid membrane.

The production of NADPH and ATP that are needed for the conversion of carbon dioxide to carbohydrate requires additional energy from sunlight absorbed by PS-1.Photosystem 1 also has an antenna of chlorophyll molecules and its own special chlorophyll a in a reaction centre. Excitation of the reaction centre of PS-1 by energy transfer from antenna pigments produces a charge separation which results in the reoxidation of the plastoquinone that had been reduced by PS-2 and the reduction of nicotinamide adenine dinucleotide phosphate (NADP) to NADPH. Electron transfer between reduced plastoquinone and the reaction centre of PS-1 occurs via a chain of electron carriers within the thylakoid membrane. Electron flow through the carriers produces a hydrogen ion gradient (pH gradient) across the membrane resulting in the production of ATP from adenosine diphosphate (ADP) and inorganic phosphate.

Dark phase

In the dark phase of photosynthesis NADPH and ATP are used for the production of carbohydrate and other carbon compounds from carbon dioxide. NADP and ADP are regenerated for activation again in the light phase. The pathway by which carbon dioxide is converted to glucose in the dark phase of photosynthesis was elucidated by Calvin and Benson in the 1950s. The key enzyme in carbon dioxide fixation is Rubisco which catalyses the addition of carbon dioxide to a 5-carbon sugar, ribulose 1,5 bisphosphate. Rubisco is a large water soluble protein in the chloroplast that accounts for about 50% of the soluble proteins of the chloroplast and about 20% of all plant protein. It is the most important protein to life on earth..

Conversion of CO2 to glucose in the Calvin-Benson pathway also involves a reduction phase that requires NADPH and a regeneration phase, requiring ATP, where ribulose 1,5 bisphosphate is regenerated to continue the fixation of CO2. The Calvin- Benson cycle runs 6 times for the reduction of six molecules of carbon dioxide to glucose. Thirteen different enzymes are used to operate the Calvin-Benson cycle. For each molecule of carbon dioxide that is reduced to CH2O, 3 molecules of ATP and 2 molecules of NADPH are required.

Carbon dioxide fixation into carbohydrate by the Calvin-Benson pathway is compromised by the competition between carbon dioxide and oxygen for the same reactive site on Rubisco. Competition with oxygen not only reduces the efficiency of Rubisco for fixing carbon dioxide but reaction of Rubisco with oxygen causes the breakdown of carbon compounds by ‘photorespiration’ and a loss of carbon dioxide. The relative rates of reaction of Rubisco with CO2 and O2 depends on the relative concentrations of CO2 and O2 at the site of the reaction in the chloroplast. Rubisco much prefers CO2 but the concentration of CO2 is much lower than the oxygen concentration.

Atmospheric carbon dioxide enters the leaf of a higher plant through small pores, called stomates on the leaf surface. Each stomate is surrounded by two guard cells and can be opened or closed by movements of the guard cells. On a hot dry day the stomates are closed to inhibit the loss of water vapour from the leaf and in so doing the entry of CO2 to the leaf is inhibited. The concentration of CO2 at the site of Rubisco declines, thus reducing the rate of photosynthesis but increasing the rate of photorespiration.

C4 Plants

Many tropical plants such as sugar cane and maize have evolved variations of the Calvin-Benson pathway for CO2 fixation that gives them an advantage in hot dry conditions. They are known as C4 Plants because CO2 is initially fixed into 4-carbon compounds. Most plants only have the Calvin-Benson pathway and are known as C3 plants. The worst weeds are C4 plants.

C4 plants have developed a different leaf anatomy. The vascular tissue is surrounded by two concentric layers of cells, an inner layer of bundle sheath cells and an outer layer of mesophyll cells. C4 plants have two types of chloroplasts located in the mesophyll and bundle sheath cells. The mesophyll cells which are close to the leaf surfaces fix carbon dioxide into 4- carbon compounds. For example, one of the 4-carbon compounds formed in the mesophyll cells is malate which then is transported to the chloroplasts of the bundle sheath cells. An enzyme in the bundle sheath cells releases CO2 from malate for re-fixation into carbohydrate by Rubisco and the Calvin-Benson cycle enzymes which are located in the bundle sheath chloroplasts. Release of CO2 from malate produces a higher concentration of CO2 in the bundle sheath cells of C4 plants than the concentration found in the mesophyll cells of C3 plants. The C4 pathway of photosynthesis was elucidated by Hatch and Slack at the laboratories of CSR in Brisbane, Australia.

C4 plants have higher rates of photosynthesis than C3 plants at high light intensities and high temperatures and lower rates of photorespiration, due to the higher concentration of CO2 relative to oxygen in bundle sheath cells. C4 plants have better water efficiency because their stomates are less open than for C3 plants.

A variant of the C4 pathway is found in several desert plant families such as the Cactaceae. It is called crassulacean acid metabolism (CAM) because it was first studied in the family Crassulaceae. The leaf stomates are closed during the day and open at night when water transporation rates are lower. CO2 is taken in at night and fixed into malate and other C4 compounds. During the day CO2 is released from malate within the plant and refixed by Rubisco by the Calvin-Benson pathway. Unlike C4 plants, CAM plants do not segregate the C4 and C3 pathways in different parts of the leaf.

Dr Keith Boardman has made major contributions to the understanding of the composition, function and development of the photosynthetic apparatus in green plants and to the adaptation of plants to their light environment, and he was the first to physically separate the two photosystems of photosynthesis. Dr. Boardman was Chief Executive of CSIRO from 1985 until his retirement in 1990. He is interested in the potential for renewable solar energy to provide a reasonable fraction of world energy usage. Other current interests include the impact of increased atmospheric carbon dioxide on plant production and the effect of climate change on ecosystems.

References

Peter Vitousek, Paul R. Ehrlich, Anne H. Ehrlich and Pamela Matson (1986)

BioScience, Vol. 36, No. 6, pp. 368-373. Human appropriation of the products of photosynthesis

Stuart Rojstaczer, Shannon M. Sterling and Nathan J. Moore (2001)

Science Vol. 294, No. 5551, pp. 2549-2552. Human appropriation of photosynthetic products

Glossary

autotroph – an organism that makes its own food.

ADP – a diphosphate of adenosine.

ATP – the triphosphate of adenosine that stores chemical energy in cells.

bundle sheath cells – a layer of cells that surround the vascular bundle in C4 plants.

Calvin-Benson cycle – a sequence of 13 proteins that convert CO₂ to sugar.

CAM – crassulation acid metabolism – a variant of C4 in some desert plants.

carotenoids – yellow carotene-related compounds.

chlorophyll a – the principal green pigment in leaves.

chlorophyll b – a green pigment slightly different chemically from chlorophyll a.

chloroplast – a small particle within a leaf cell and the site of photosynthesis.

C3 plant – a plant that has the Calvin-Benson cycle to convert CO₂ to sugar.

C4 plant – a plant that first converts CO₂ to compounds with 4 carbon atoms.

electron carriers – organic molecules containing iron or copper that transfer electrons.

guard cells – cells that cause the opening and closing of stomates.

mesophyll cells – a layer of cells close to the surface of a leaf.

Pg – petagram equal to 10¹⁵gram or 10⁹metric tonne or one Gigatonne.

photorespiration – oxidation of organic molecules driven by light in photosynthesis.

photosystem 1(PS-1) – chlorophyll-protein complex that reduces NADP.

photosystem 2(PS-2) – chlorophyll-protein complex that splits water molecules.

phycobilin – a pigment in red and blue algae.

phytoplankton – marine algae(microscopic plants).

plastoquinone – a lipid-like quinone molecule.

rubisco – ribulose bisphosphate carboxylase, the catalyst for the fixation of CO₂.

stomata – a small opening in the surface of a leaf.

thylakoid – an internal membrane of the chloroplast.

This paper as a 161KB pdf

Colin Groves

The molecular clock seems to indicate that humans separated from chimpanzees some 7 million years ago, with a possible range of about 6 to 8 million. The earliest fossil plausibly assigned to the human lineage is Sahelanthropus tchadensis from the Koro Toro district of Chad, although some authors have misgivings about it, and it remains possible that it in fact denotes a time before the separation of human and chimpanzee lineages, or it may even be a member of the gorilla lineage. It is represented by a magnificent, but distorted, cranium (it is the distortion that is the main source of the misgivings), plus a few other fragments.

From Lukeino in the Kenya Rift Valley comes a more widely accepted fossil taxon, Orrorin tugenensis, one of the few proto-human fossils known almost entirely by post cranial bones, and identified as being part of the human clade mainly by incipient bipedal features of the femur. A few jaw fragments and teeth also represent this species. It is interesting that from the same deposits come a few teeth that are the first plausible fossil representatives of the gorilla lineage: it has always seemed odd that we know plenty of human ancestors and collaterals, but no gorillas (and there are still no chimpanzees until we get to a mere quarter of a million years ago). Orrorinis nearly 6 million years old; a long-known but still unnamed jaw from the Rift Valley site of Lothagam is 5.5 million; Ardipithecus kadabbais somewhat over 5 million; Ardipithecus ramidusis 4.4 million; and shortly after that we begin to get remains of the big-toothed fossils called australopithecines.

But these ‘pre-australopithecines’ are now becoming better known, and actually they seem to form a nice graded series, through which we can see the beginnings of bipedal specializations developing into a fully fledged upright locomotion, and we can see the canine teeth becoming smaller, though they are still larger in the males than in the females. They all had relatively shorter, thicker jaw bodies than ‘apes’, but the enamel coating on their cheekteeth was thin like a chimpanzee’s. The coming of the australopithecines (first known by fossils from southern Ethiopia, a little over 4 million years ago) seems to represent a somewhat new direction, with very large molar and premolar teeth coated with thick enamel, still smaller canines, and fully-fledged upright stance; it is unclear whether they were derived from Ardipithecus ramidusor both were derived from an earlier common ancestor.

Australopithecines were very diverse. There was no ‘onward and upward’: they separated into many different species, some of them restricted geographically and replaced by relatives in other geographic areas, others apparently specializing in different modes of exploitation of the environment. They are often divided into several different genera:Australopithecus, Paranthropus, Praeanthropus, Kenyanthropus, and certainly there were a number of different species, perhaps as many as 10 or even more over the 3 million years in which ‘australopithecines’ shambled around Africa. All of them had relatively small canine teeth (the size of the canines can be seen reduced over time), small brains (more or less chimpanzee-sized, the cranial capacity about 380-520 cc), and protruding muzzles (prognathism). The most specialized of them, the ones often placed in a distinct genusParanthropus, had tiny front teeth and huge cheekteeth, and fed on heavy vegetation; stable isotope analysis shows that they moved between woodland and river valley habitats, and there is now an interesting argument that they may have eaten termites, inserting sticks into the mounds like chimpanzees do.

Though there is absolutely no doubt that the australopithecines stood and walked upright, they may still have been capable of climbing in trees and even of walking quadrupedally using the knuckles of their hands like chimpanzees. The problem is how we want to interpret the primitive characters they still possess in their skeletons, such as their curved phalanges (finger and toe bones) and the knuckle-walking features in their wrists: are they mere relicts of an evolutionary past when they clambered through the branches and knuckle-walked along the ground, or did they persist in these behaviours sometimes? Certainly, the knees were ‘valgus’, meaning that they were placed under the centre of gravity of the body, because the thighs sloped in from hip to knee; the pelvis was low and broad; and the great toe was apparently not very divergent, if at all. Even if we see them as entirely bipedal, interpreting their other locomotive features as mere relicts, we should not think of them as walking entirely like us: aspects of the pelvis indicate that their body did not rotate as they walked to the same degree as ours, and their legs were short, and they did not therefore have the easy, loping, striding gait that we have.

Around 2.3 million years ago there is evidence of a new type of proto-human, with a shorter, more parabolic palate, a fully upright head posture, and longer legs. I say ‘a’ new type, but in fact it is the site of Hadar that yields the palate, Sterkfontein that has the basicranial specimen, and from Bouri come the limb bones: it is tempting to put them together into a single creature, and perhaps add the Chemeron temporal bone with its suggestion of increased brain size, but at present these disparate fragments do not permit us to do this! It is not until we get evidence of ‘habilines’ at 2 million years ago in East Africa, of which the best-known species is Homo habilis, that we have the first evidence of a creature with somewhat increased brain size (cranial capacity 510-680 cc), head balanced on the spine in the modern fashion, shorter jaws and smaller cheekteeth. Even then, the postcranial skeleton is poorly known, but the latest evidence does suggest relatively longer legs than any australopithecine.

The earliest proto-human species with a striding gait is Homo ergaster, so far known for sure only from the Lake Turkana sites of Koobi Fora (on the east side of the lake) and Nariokotome (on the west side) from 1.8-1.4 million years ago, but several skulls and a nearly complete skeleton, the ‘Turkana boy’, are known. The brain size was larger than any previous species (cranial capacity 800-900 cc), there were thin but protruding brow ridges, the face was much less prognathous, and for the first time there was a somewhat protruding nose. The pelvis was virtually modern in form, and in most respects the skeleton was modern, although the femur was not precisely like modern humans.

For a long time it was assumed that the descendants of Homo ergasterdid not extend their range outside Africa until about a million years ago, or even less. The earliest species to live outside Africa was thought to be Homo erectus, known from several fossil sites in Java; this species had a low, angular thick-walled braincase, with very thick, protruding bar-like brow ridges. Indeed, traditionally all proto-humans except for the habilines were placed in Homo erectus, which was envisaged as the ancestral species to Homo sapiens,but over the past five to eight years all this has changed. It is realized now that the old ‘catch-all’ usage of Homo erectusis misleading: the Java species could certainly not be ancestral to modern humans, and unless we clearly distinguish the different populations (probably different species) at one time lumped into erectusthere would never be any hope of disentangling evolutionary lineages.

But another, quite unexpected, turn of events has forced an even more radical rethink: the discovery of the extraordinarily rich site of Dmanisi, in the Republic of Georgia. Not only is this outside the tropics, at a strikingly early period (1.7 million!), but the fossils from the site are actually more primitive even than Homo ergaster– intermediate, in fact, between that species and Homo habilis. So far, as of mid-2006, as many as five excellently-preserved skulls have been found, as well as several jaws (most of them fitting the skulls) and postcranial bones, not yet fully described. They had small brains, about 650-750 cc, thin protruding brow ridges, considerable prognathism, the beginnings of a protruding nose, and an unexpected degree of sexual dimorphism: when a new jaw was discovered in 2003, it was so much bigger than those previously known that there were doubts whether it was the same species, but it seems now clear (because the recently discovered skull that fits it is not very different from the other skulls) that it is simply a very large male and the other jaws were mostly small females.

How many times did populations of early humans leave Africa and spread to Asia and Europe? It is still unclear, but it seems at least three times. We should not think of these early proto-people as getting the wanderlust, or being forced to leave for some reason; they were animals like any other, and animals just expand their range as far as suitable habitat extends, to the point where geographic barriers get in the way. The difference in this case is that the proto-human ecological niche seems to have been broadening progressively, so that there was a wider range of habitats that were suitable for them.

What, then, in the days of Homo ergasterwas the human ecological niche? Their remains are found in lightly wooded or savannah habitats, as the associated fauna tells us, but generally in the vicinity of streams or lakes. Here they probably ate vegetable matter such as fruit, seeds, stems and underground plant parts, and certainly ate meat; the meat, though, was most likely scavenged in the main, because the cut-marks of their stone tools frequently overlie those of the teeth of big cats and other carnivores.

They made these stone tools, of course, as they had done since the time of their presumed ancestor, Homo habilis; we can presume that australopithecines and even the ‘pre-australopithecines’ used stone to pound hard foods, and modified vegetation and wood to use as probes, digging sticks and even weapons, because chimpanzees do all that and our ancestors would presumably have been capable of no less, but modifying stone before it is used as a tool is more than chimpanzees do. The first definite stone tools occur in 2.3 million-year-old levels at Hadar, alongside the earliest known palate of a habiline. By 1.9 million years ago, at Olduvai Gorge, some proto-human, presumably Homo habilis, was collecting suitable stone from as much as 12 km away; chimpanzees certainly bring stones to crack nuts from several hundred metres away, but 12 km seems a fairly major intellectual achievement.

There is no evidence that these early stone tools, known as pebble tools, were anything but ad hoc; they would pick up one of their collected stones and strike flakes off it until they had one that they could use. The early out-of-Africa proto-people used pebble tools as well; tools shaped to a mental template, to produce a deliberately shaped product such as a hand-axe, began to appear about 1.4 million years ago, and spread through Africa, and eventually into Europe, but in Asia they got no further than the Indian subcontinent, and that not till much later.

By about 600,000 years ago, a big-brained species known as Homo heidelbergensishad spread throughout Africa, and when the climate permitted throughout much of Europe as well. For this was the time of the ice ages; since a million years ago or more, periodic spread of the polar ice sheets had made much of the high latitudes uninhabitable by humans, and they spread and receded again at approximately hundred thousand year intervals. When they receded, Homo heidelbergensisspread north into Europe; when they came down again, the populations were compressed back into Africa. But there came a time when evolving cultural adaptations permitted them to stay in Europe and ride out the bitter cold, and in this sort of environment they changed, developing bigger brains (as big as ours), big facial sinuses and huge noses, and a characteristically stocky build, people we call the Neanderthals, Homo neanderthalensis. Remains of the Neanderthals are known from all over Europe and the Middle East from about 300,000 years ago. Meanwhile in Africa, a new type was emerging as well: people with round high braincases, short faces and long limbs – the first Homo sapiens.

For a long time, these two species were geographically separated. In the caves of northern Israel, dating between 60,000 and 120,000 years ago, remains of both are found, but not in the same layers. Associated fauna shows that, when the climate was cold, the Neanderthals lived there; when it was warm, the Neanderthals retreated north, and Homo sapiensspread into the region from Africa. But the time came when some accident of history – the invention of the blade technology of stone tool making, perhaps – gave our species an advantage, and Homo sapiensspread on, north into Europe and east into the main mass of Asia. From 40,000 years ago, modern humans spread westward through Europe, and the Neanderthals crumbled before them; we need not invoke warfare or anything like that: simply, for some reason, the moderns did the human thing just slightly better than the Neanderthals, and their populations increased and the Neanderthals’ decreased. The last of the Neanderthals hung on until 30,000 years ago or less in Spain and Portugal, and the skeleton of a five year old child found in Portugal, dating to 25,500 years ago, has been identified (admittedly very controversially) as a hybrid.

And as modern humans spread east, the remnants of other species gave way before them as well. It is claimed that ‘Solo Man’, a direct descendant of Homo erectus, survived until 30,000 years ago in Java; by this time modern humans were already present in the region (the first Homo sapiensremains are 40,000 years ago, from Niah in Sarawak, but moderns must have been there still earlier, because Australia was occupied by 50,000 years ago). And there was someone else present in the region as well – someone whose presence was totally unsuspected until 2004. Homo floresiensis, the Hobbit from Flores, four islands to the east of Java, separated from anywhere else by deep water.

People have found it hard to come to terms with this Hobbit. A humanlike creature one metre tall, with a cranial capacity of 400 cc, and not only no chin but strong internal buttressing of the jaw; with short stout legs and long feet; known from a nearly complete skeleton and the isolated bones and teeth of a dozen individuals ranging from 90,000 to 12,000 years ago. There have been all sorts of extravagant and implausible claims that they were actually dwarfed, pathological, or otherwise defective modern humans: microcephalics, cretins or whatever. Ockham’s Razor has been notable by its absence. Detailed analyses by different sets of authors seem to be settling on an interpretation that Homo floresiensiswas a descendant of a late australopithecine or perhaps of Homo habilis, meaning that there was a dispersal of a proto-human species out of Africa even before Dmanisi. And why not? From now on, archaeologists working in subtropical and tropical Asia will be alert to the possibility that the earliest occupants of their sites may be these habilines that ended up in Flores.

They were there then; they are not there now. Homo sapiensstands alone. But Homo sapiensis descended from animals, which lived like animals, evolved like animals, speciated and diversified like animals. It is as well to remember this, and to draw the inevitable conclusion: Homo sapiensis still an animal.

Further Reading

Cameron, David W. & Colin P. Groves. 2004. Bones, Stones and Molecules. Elsevier Academic Press.

Foley, Jim. Fossil hominids: The evidence for human evolution.
http://www.talkorigins.org/faqs/homs/

Glossary
Fossil taxon: a taxon (species, genus or whatever) known only as fossils.
Clade: an evolutionary branch, consisting of an ancestor and all its descendants.

Colin Groves holds a PhD in primatology from the University of London, and has worked on the taxonomy and evolution of primates and other mammals, and on human evolution. He is at present involved in a series of projects concerned with revising our knowledge of the classification, biogeography and phylogeny of wild cats, red pandas and weasels, of rhinos and antelopes, and of primates.

This paper as a 130KB PDF

Stephen Boyden

Uniformities
Biodiversity
Food intake in plants
Food intake in animals
Reproduction
Comment
Further reading

We have only to look around us anywhere in the natural environment to be struck by the amazing diversity among living organisms – diversity in habitat, size, shape and colour; and, among animals, diversity in means of locomotion and patterns of behaviour. Animal species also differ widely in their food sources, and in their resistance to heat, cold, dryness and wetness; and some are at home on the land, some in the water, some in the soil, and some in the air. Each is adapted, in its inheritable characteristics, to its own particular ecological niche.

It is impossible to state precisely how many different kinds of life now exist on Earth, but it has been roughly estimated that there are some 7 to 15 million species of living organisms (excluding bacteria, fungi and viruses). Of these, around 400 000 are plant species and around 50 000 are vertebrates.

Uniformities

Underlying all this diversity, however, there are some remarkable and essential uniformities. One of these fundamental universals is the fact that all forms of life depend on a continual supply of energy. Except in the case of a small proportion of microbial organisms, this energy was initially captured from sunlight by photosynthesis in green plants, converted into chemical energy and stored in organic molecules.

There is also a basic similarity in the complex chemical processes by which this energy is used in living cells, be they animal, plant or microbial. For example, a common denominator at the molecular level is adenosine triphosphate (ATP) which, in every kind of living organism, plays an essential part in the chemical reactions involved in the storage of energy and its eventual release ­ for example, in the synthesis of complex molecules or the contraction of muscles.

The organic molecules of which organisms are made up also share the same basic characteristics right across the board. These molecules fall into four classes: carbohydrates, proteins, lipids (fats) and nucleic acids. However, within these four main classes there is immense diversity. In the case of proteins, for example, every species of animal and plant has very many different proteins with different functions ­ for example, as enzymes, hormones, or playing specific structural roles ­ and the proteins of each species are distinguishable from those of all other species. Indeed, subtle differences exist in the structure of proteins between individual members of the same species. This is why skin, or other organs, can only rarely be successfully grafted from one individual to another (except in the case of identical twins), unless special steps are taken to depress the immune system of the recipient. The rejection of the tissue graft from another individual is due to the fact that the immune system recognises the cells of the donor as "foreign", and consequently sets up an inflammatory response which ultimately destroys them.

Genetic inheritance - Another universal is the fact that all life forms, with the exception of sub-microscopic viruses, have a cellular structure ­ ranging from single-celled organisms, like bacteria and amoebae, to the large multicellular plants and animals, which may be made up of hundreds of billions of separate cells with many different functions. But every one of these multicellular animals, and most of the multicellular plants, begin life as a single cell, formed by the union of two cells ­ the ovum and the sperm.

This leads us to note another universal among living organisms, and that is the means by which genetic information is passed from parents to their progeny, providing the instructions that result in the new organisms developing and functioning as members of the species to which their parents belong, and that determine all their other inherited characteristics.

The essential agent in this process is the genetic material of the cell, deoxyribonucleic acid (DNA). In animal and plant cells chains of DNA are located in the cell nucleus, and in this situation (and, in some laboratory situations, outside the living cell) DNA is itself capable of self replication. It contains, in coded form, most of the information necessary for the formation of the new individual.

The inheritable characteristics of any organism are determined by the arrangement of four nucleotides (cytosine, thymine, adenine, and guanine) in the genes, which are discrete areas or regions on the DNA chains.

Sexual reproduction - Almost universal among plants and animals is the involvement of the sexual process at some stage in the reproductive cycle. This consists of the fusion of two separate cells (gametes) which, in the case of multicellular organisms, usually come from two different individuals (but in some species, from different parts of the same individual). In some very simple organisms the two gametes may be identical, but in all higher species of plants and animals they are clearly different. One, the male gamete, or sperm, is motile. The other, the female gamete, or ovum, is larger and sessile. The fusion of the two cells results in the new fertilised egg, or zygote, which contains twice the amount of DNA contained in each of the gametes. However, there is a mechanism, known as meiosis, by which the amount of genetic material is halved at a specific stage in the formation of the gametes as a consequence of which is that the total amount of genetic material does not double continually at each generation.

The fertilised egg thus contains genetic material from two different sources (i.e. from both parents). Since it is very unlikely that the material from each parent will be identical, it follows that the offspring will be different, even if only slightly, from either parent.

As a result of this sexual process, the genetic material in a population is being constantly reshuffled. From the evolutionary point of view, the importance of sexual reproduction lies in the fact that, unlike in asexual reproduction, the precise genetic make-up of the new individual is different from that of either parent. This has the effect of maximising the number of genetic combinations in the population, thereby enhancing the potential of the population to adapt to environmental change though natural selection.

Gene mutations - While the mechanism of sexual reproduction explains the continual rearranging of genetic material in populations, it does not explain how entirely new genetic characteristics come into existence. The process responsible for such change, known as mutation, involves a chemical change in a gene that is perpetuated when the gene replicates in cell division. The change then affects the particular characteristic of the organism for which the gene is responsible. Mutations are normally rare events, but their frequency can be increased by certain physical and chemical agents, such as ultraviolet light, radioactive radiation and mustard gas.

The great majority of mutations are deleterious, so that cells that carry them do not survive. Occasionally, however, a mutation arises which, by chance, increases the likelihood of the organism surviving and successfully reproducing in the habitat in which it lives.

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Biodiversity

Despite these fundamental uniformities, the processes of evolution have given rise to an amazing variety of structural forms, physiological mechanisms and ways of life. It is not possible here to attempt even a summary of all the kinds of adaptations to different habitats found in the plant and animal kingdoms. Let us simply use a few examples to give some idea of the extent of diversity that exists and to illustrate some important biological principles. We will consider diversity with respect particularly to two main aspects of life: food intake; and reproduction.

Food intake in plants

The range of ecological niches exploited by plants is vast, and is reflected in the wonderful array of different forms of vegetation that can be found, for instance, in the deciduous and coniferous forests of the northern hemisphere, in the dense evergreen forests of the tropical and sub-tropical zones, in the eucalyptus and acacia forests of Australia, in the mountainous terrains, savannah country, low-lying marshlands, deserts, heathlands, and sand-dunes of Africa, Australia, and South America, as well as in the meadows of the established agricultural systems in temperate regions of the world.

Each plant form is adapted, through evolution, to certain conditions of temperature, humidity, soil quality, soil wetness, light and wind.

While some water is essential for the survival and growth of all plants, enormous variation exists in the amount of water that different plants need. Some forms, like most reeds and bulrushes, cannot survive in soil that does not have a high water content, while others are adapted to extraordinarily dry conditions. Plants found in dry habitats often have small, leathery leaves. An extreme example is provided by the desert cacti in which the leaves are hard, spiny structures which do not support photosynthesis. In these plants the photosynthetic process takes place in the fleshy stems, which are also organs for storing water. Their water content may account for up to 98 percent of their weight.

There are many other kinds of adaptation in plants to dry conditions. One of these takes the form of very short life-cycles. Parts of the Australian desert may receive a reasonable rainfall only once in every few years. When this occurs, the previously parched and apparently lifeless ground suddenly becomes an amazing mass of small flowering plants, and in a very short time seeds are produced. If there is no further rain, the soil soon returns to its state of desiccation, but containing myriads of drought-resistant seeds which lie dormant until next time it rains.

In most leafy plants the size of the pores, or stomata, on the leaves can be varied in response to changes in the moisture content of the soil and the humidity of the atmosphere, thereby controlling the rate of water loss by evaporation. In some plants that live naturally in dry regions, the stomata are permanently sunken into the surface of the leaf, minimising evaporation, while in others the leaves are covered with hairs which have the same effect. In many plants the leaves fold up when conditions become dry, and in some forms the leaves fold regularly after dark and sometimes in the late afternoon. In most plants only about 1 or 2 percent of the water taken up by the roots is used in photosynthesis: the rest is released through the stomata into the atmosphere - a process known as transpiration.

A particularly interesting adaptation to nutrient deficiency in soils is seen in the carnivorous plants, of which there are at least 350 different species. These plants are usually found in swamps, bogs and peat marshes where acids have leached the soil of nutrients; their prey may consist of insects and other invertebrates and sometimes even small birds and amphibians. The sundews, for example, are very small plants, usually not more than 5cm across, and they have tentacles on the upper side of the leaf which secrete a clear sticky fluid that attracts insects. As soon as an insect is caught by one tentacle, the others bend inwards towards it, so that the animal is thoroughly trapped. The tentacles also secrete enzymes which digest the insect tissues, and the soluble nutrients are then absorbed by the leaf surface. Among other carnivorous plants is the well-known Venus flytrap, which occurs naturally only on the coastal plain of North and South Carolina, in North America. Unlike carnivorous animals, carnivorous plants do not use their prey as a source of energy, but rather as a supplementary source of certain nutrients, especially nitrogen and phosphorus.

A much more common way of acquiring nitrogen is that which operates in the legumes, like clovers, vetches, lucernes, peas, beans, and acacias, and which involves a symbiotic relationship between the plant and certain nitrogen-fixing bacteria. When the plants are seedlings their root hairs are invaded by the bacteria (Rhizobia), and eventually these give rise to small nodules in which the bacteria live and multiply. These micro-organisms fix free nitrogen and release it in the form of ammonia, which combines with carbon compounds in the plant cells to produce amino acids.

In agricultural systems the beneficial effects of growing legumes has been appreciated for at least two hundred years. Some of the fixed nitrogen is released into the soil around the legumes and so becomes available to other plants. If the leguminous plants are ploughed back into the soil, much of the nitrogen incorporated in the tissue of the legumes becomes available for other crops. A crop of lucerne ploughed back into a field may add as much as 350 kilograms of nitrogen to the soil per hectare.

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Turning to the procurement and assimilation of food in animals, the basic arrangement of the digestive tract (a single mouth, a stomach and intestines containing digestive juices, and a single anus) is common to all multicellular animals, from mosquitoes to elephants, with the exception only of some simple forms like the sponges, coelenterates and flatworms. The extent of variation on this common theme, however, is enormous.

First, the great range of different kinds of food sources has resulted in wide variation in the structure of the mouth parts. The following examples illustrate this point: the grinding molars of herbivores (e.g. ox, horse); the sharp cutting teeth of carnivores (e.g. dog, tiger); the beaks of the sparrow and the pelican; the sucking mouthparts of leeches; the powerful biting and chewing jaws of the preying mantis; the proboscis of the mosquito; the fly-catching tongue of the chameleon; and the simple oral cavity of the earthworm.

Digestive organs - There is also great diversity in the various organs concerned in the digestive process, and in the biochemical properties of the digestive juices. Because of the specificity of these adaptations, if animals are forced to feed on a diet that is significantly different from that to which they are adapted through evolution, it is likely that they will show signs of ill health. Tigers will not last long on a diet of honey, and bee larvae cannot survive on a diet of meat.

The following few examples illustrate the range of adaptations in the internal digestive organs. Termites eat mainly wood. However, like other animals, they do not produce any enzymes in their digestive juices capable of breaking down cellulose, which is the chief component of their diet. They are entirely dependent for their nutrition and survival on certain protozoa which they harbour in the stomach and which produce an enzyme that splits the lignin into soluble carbohydrate molecules which can be utilised by the termite.

Birds' digestion - There is wide variation in the structure and physiology of the gastro-intestinal tract among birds, depending on the kind of diet to which they have become adapted through evolution. In most birds the lower end of the oesophagus swells into a large storage chamber, the crop, where the food remains, sometimes for as long as two days, until the stomach can accommodate it. In pigeons the crop takes the form of a large double sac which not only stores grain, but which also secretes 'pigeon's milk' for feeding the young birds. Crops are generally prominent in grain-eating birds, allowing them to swallow a relatively large volume of food in a hurry, so shortening their time of exposure to predators.

The actual stomach of birds consists of two parts, the anterior glandular stomach, which secretes digestive juices, and the posterior muscular stomach, or gizzard. The gizzard is especially well-developed in grain-eating birds, and it is lined with horny plates or ridges that serve as millstones for grinding the food. This process is often furthered by the abrasive action of small pieces of grit that the birds have swallowed. The gizzard of the domestic goose may contain 30 grams of grit. In carnivorous birds the gizzard usually has much thinner walls and has a completely different function. In owls, gulls, swifts, grouse and some hawks it operates as a trap that stops sharp bits of bone and other non-digestible fragments from passing on through the alimentary canal. This material is rolled up into elongated 'pellets' which are regurgitated through the mouth.

Ruminant digestion - A further example of an alimentary adaptation to a specific kind of diet is provided by the four 'stomachs' of cattle, giraffes and other ruminants. These animals tear the leaves off the plant they are eating with their incisors and swallow them almost immediately, without making any attempt to chew them up. The food bypasses the 'first stomach', or rumen, and goes directly to the smaller 'second stomach' or reticulum, where it is compacted into balls. At a later time, when the animal has stopped feeding, these balls, which are referred to as the cud, are regurgitated to the mouth. The cud is then properly chewed by the grinding action of the animal's molars, before being swallowed a second time, this time to be retained in the rumen. This organ is very large, and represents about 80 percent of the total volume of the four stomachs. It is colonised by bacteria and protozoa which not only break down cellulose, as in termites, but also synthesise proteins, using urea and ammonia as nitrogen sources. Some of these micro-organisms pass on down the alimentary canal and are themselves digested, so contributing to the animal's intake of amino-acids. Some of the products of the fermentation are absorbed directly by the lining of the rumen. The rest of the food passes into the omasum, or third stomach, which basically functions as a strainer, and then on to the abomasum. This is the true stomach, where peptic enzymes are secreted. Anatomically, the rumen, reticulum and omasum are actually expansions of the oesophagus.

Finding food - There is also a great deal of variation among animals in the ways that they find and procure their food. A few examples will illustrate the extraordinary range of different kinds of adaptation.

Many species locate their food simply by going around looking for it, in much the same way as we would ourselves, using especially the senses of sight, smell and hearing. Clearly there is a broad distinction between the techniques of herbivores and carnivores, in that the latter (except in the case of scavengers) have not only to locate their food source, but also to catch it. Some groups of animals, however, have very specialised modes of food location and procurement. Bats, for instance, have evolved a special mechanism for detecting their prey in the night sky, known as echolocation. It involves the emission of sounds at very high frequencies and the detection, by means of highly specialised listening devices, of echoes of these sounds coming from objects in the environment. When the returning signal indicates that the object detected is of an appropriate size and is moving in the air, the bat flies rapidly and unerringly towards it, and catches it. The bat is able to discern from the signal whether the object is flying towards or away from it. A similar mechanism has evolved independently in dolphins which also emit ultrasonic pulses, and the pattern of returning echoes provides them with a picture of the world around them.

In some carnivorous animals that feed in water, special receptors have evolved that detect very small electric impulses generated by the muscular movements of their prey. The platypus, which is effectively blind under water, detects small crustaceans and worms that form its diet in this way. Frog tadpoles and some fish make use of similar mechanisms.

Ant 'farmers' - We cannot leave the subject of food acquisition in animals without reference to the farming practices by certain kinds of ant that live in tropical and sub-tropical regions on the American continent. Some of these species collect pieces of leaves or flowers from living plants and carry them back to the nest, where they cut them up into smaller pieces and mix them with saliva and faeces. The ants spread out the resulting compost in an underground garden, and then place pieces of mycelium from a certain kind of fungus on top of it. The fungus, digesting and deriving nourishment and energy from the cellulose in the leaves or flowers, grows profusely. As the mycelium grows, the ants continually make cuts in it, and at the site of each cut the fungus develops a nodular proliferation. These nodular proliferations are eventually harvested by the ants as a major food source. Some other more primitive ants in the region make use of the same principle, but use insect faeces, or dead insects, as a substrate for the fungal mycelium instead of plant material.

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Reproduction

The ability to reproduce and so perpetuate the species is, of course, an essential feature of all groups of living organisms. Reproduction ranges from the simple division of one-celled organisms through to the very complicated structural, physiological and behavioural processes that occur in higher plants and animals.

Asexual reproduction - Despite the underlying uniformities at the molecular level mentioned at the beginning of this section, the actual details of the processes of reproduction at the level of whole organisms vary enormously. First, let us note the all-important distinction between sexual and asexual reproduction. In asexual reproduction there is only one parent, which splits, buds or fragments to give rise to two or more new individuals, each of which have hereditary characteristics identical with those of the parent. Asexual reproduction is common among simpler forms of life, including bacteria, algae, fungi, mosses, protozoa, coelenterates and flatworms. In the case of the last group, if the animal becomes fragmented into several pieces, each may develop into a new whole animal. If a starfish is cut in two, each part will regenerate tissue to form a complete new starfish.

Among plants, even the higher seed plants (angiosperms) are capable of reproducing asexually. Some species, such as English elms and Lombardy poplars, may propagate by putting out 'suckers', so that new trees grow up from the distal roots of the parent trees. Reproduction by rhizomes (actually stems growing laterally underground) and by tubers is also common, as horticulturists have appreciated for many thousands of years. Propagation of plants by means of cuttings is another example of asexual reproduction. Indeed, asexual reproduction also occurs in higher animals, including humans, when a newly fertilised egg divides in the uterus to give rise to two or more genetically identical eggs, each of which develops as an independent organism. Today, as an outcome of scientific advances, it is now possible to bring about asexual reproduction artificially in mammals by means of cloning techniques.

Turning to sexual reproduction, we have already noted some basic differences between the simpler, more ancient plants, such as mosses and ferns, and the more recent conifers and flowering plants. Let us look at a few of the adaptations that have evolved in this last group.

Pollinators - The most striking feature of the reproductive processes of the flowering plants is the fact that, while the wind sometimes plays a part in transporting pollen from flower to flower, the great majority of species rely entirely on insects, or in some cases on small birds or mammals, to bring about pollination. For this to work, the insects have first to be attracted to the flowers, so that they pick up pollen and later drop it off when they visit other flowers of the same species, where it can bring about fertilisation. The basic attractant for insects in the great majority of plants is food, in the form of nectar, which is produced at the base of the flower solely for this purpose. Another feature of the adaptation of the flowering plant is the development of petals, which are often displayed conspicuously and in bright colours, signalling to insects the presence of nectar.

While this basic pattern is very common, there are many interesting and sometimes bizarre variations on the general theme. The orchids, as Darwin noted in his remarkable book on these plants, are especially interesting from this point of view. In one species the shape and colour of the flower bears a strong resemblance to the female of a particular species of wasp, complete with eyes, antennae and wings. It even gives off an odour which is the same as that emitted by a female wasp that is ready to mate. Male wasps, deceived by this arrangement, attempt to copulate with the flower. In doing so, they pick up pollen, which they inadvertently deposit on the next flower with which they try the same thing.

Another interesting example is a plant known as the dung lily, which gives off an odour similar to that of herbivore dung. When a dung beetle happens to fly overhead, it responds to the dung-like stimuli by dropping head first into the funnel-shaped flower. Because the inside of the flower is lined by small hairs pointing downwards, the beetle is unable to climb out, and if it happens to be carrying pollen from a previous encounter with a dung lily, some of this will come off and fertilise the ova. By morning, the flower tips over and the one-way hairs no longer prevent the beetle from escaping ­ which it does. On the way out it picks up some pollen that had not been available when it entered.

Aquatic animals - In multi-cellular animals, two main mechanisms exist for achieving union of egg with sperm. The first operates only in the case of animals that live, or at least mate, in water, and it involves the male liberating sperm into the water in the region where the female has recently laid her unfertilised eggs. Usually this act is preceded by certain courtship behaviours which ensure that the male is at the right place at the right time. This method operates in most marine animals, from molluscs to true fishes, as well as in amphibians, which return to the water to mate. In frogs, for instance, the male arranges himself on the back of the egg-laden female, keeping firmly in place by means of special clasping pads on the front of his forelimbs. He remains in this position until the female begins to lay her eggs, at which time he ejects spermatozoa into the water, a small proportion of which find, and unite with, ova.

The pattern in newts and salamanders is somewhat different. For example, in the common newt of north-western Europe, Triturus vulgaris, the male courts the female with a dance display involving a rapid waving movement of the end of his tail, which is turned back on itself, and so points forward. When the female is appropriately aroused, apparently partly as a result of a hormone discharged into the water from the male cloaca, the male newt deposits a mucilaginous bundle of spermatozoa, which the female picks up with her hind limbs and inserts into her cloaca, so that fertilisation takes place internally.

Land animals - The main mechanism for bringing sperm and eggs in contact in land animals involves the insertion of a male copulatory organ into the genital tract of the female, and the ejection from the male organ of sperm, which then swim their way to the ova. This mechanism exists in most insects, in some birds, and in all reptiles and mammals, although different procedures operate in worms and some arthropods.

The reproductive pattern of the earthworm is particularly complex. Earthworms are hermaphrodite, and during mating the two worms, heading in opposite directions, lie with their ventral surfaces in opposition and are held together by a sticky secretion. Each worm donates sperm to the other, and these are temporarily stored in a seminal receptacle. After the worms have separated, a glandular ring of thickened skin called the clitellum secretes a membranous cocoon. As the worm frees itself from this cocoon, it discharges into it both ova produced in its own body as well as the sperms contributed by the other worm. As the cocoon slips off the worm, its two openings constrict, and the fertilised eggs then develop inside it to produce new worms.

Another interesting mechanism has been observed in certain species of peripatus, which are curious caterpillar-like animals that live in moist forests in Africa, Asia, Australia and South America. They have many pairs of legs, and they share characteristics of both the annelid worms and arthropods. In some species of peripatus, males have a special protuberance on their head which is used to carry around a drop of semen, as the animal searches for a female. When a female is found, the male deposits the semen somewhere on the surface of her body, and a cellular reaction immediately takes place inside the female, as a result of which some specialised cells in her body transport the sperm to the ova in the uterus.

Spiders - Reproduction in spiders is rather similar to the first part of this peripatus procedure. The male produces a ball of sperm-containing material which he picks up with one of his pedipalps, which are limb-like structures situated just in front of his four sets of legs, He then sets out in search of a female which, in most cases, he must approach with considerable caution, identifying himself by certain species-specific signals in order to avoid being attacked and eaten. On reaching the female, the male inserts the spermatozoa into the female genital tract. In most cases, he then quickly makes his get-away, although in some spiders the female consumes the male as soon as mating is completed.

Attracting mates - A great variety of procedures exist among different animals for ensuring that males and females find each other for mating purposes. In many instances the female gives off a specific odour which attracts males. In some moths, the males are exquisitely sensitive to such odours ­ responding when there are only about a hundred molecules of the specific substance per millilitre of air. It has been estimated that, in some kinds of moth, the male can detect a female over 4000 metres away, if a gentle breeze is blowing in the right direction.

In other species, the male attracts the female to a particular place or territory by emitting a distinctive call. This pattern is common among birds and frogs. In some bird species, the peacock and the Australian lyrebird being notable examples, males attract females by extending and displaying their tail feathers. In bowerbirds the males achieve the same objective by decorating their ‘bowers’ with all sorts of colourful objects.

In the great majority of mammals, from rats, mice and shrews, to dogs, zebras, elephants and monkeys, females undergo a hormonally controlled cycle, and they are sexually attractive, or receptive, to males only at the certain periods that coincide with ovulation. Biologically, the important consequence of this mechanism is that mating takes place only at times when fertilisable ova exist in the female genital tract. An outstanding exception to this generalisation is Homo sapiens, in which females can be sexually attractive to males at all times, and in which female receptivity is not restricted to a short period in the hormonal cycle.

Mothers' milk - A feature relevant to reproduction and common to all mammals is the production of milk in the mammary glands of females, which is the only source of food for their new-born offspring. Only one species of mammal is known in which new-born animals can survive without milk, eating solid food immediately after birth, and this is the guinea pig. Nevertheless young guinea pigs do drink milk from their mothers if it is available. At the other extreme is the young grey kangaroo, which weighs less than a gram when it is born and which, although it makes its own way from the urogenital opening of the mother to the pouch, is otherwise completely helpless. Once in the pouch it immediately becomes attached to one of the nipples, and it does not leave the pouch, even for short periods, for 9 months.

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Comment

The examples given above only touch the surface of the vast range of different life forms that exist on earth. The shelves of science libraries hold countless volumes providing detailed information on the structural, physiological and behavioural diversity encountered among living organisms. And apart from all that has already been described, there is much more yet to be discovered.

Appreciation of this biodiversity is crucial to our understanding of life, of the human place in nature and of the urgent need to support, rather than disrupt, the complex web of life on which we depend and of which we are a part.

An outstanding feature of the present day is the extraordinary rate of loss of biodiversity due to the activities of humankind. Extinctions resulting from human activities have been estimated at up to 140 000 species a year. At this rate about half the existing species will be wiped out in 70 years.

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Further reading

For further information see our paper Loss of biodiversity

and

E.O.Wilson, 1989, Biodiversity. National Academies Press, Washington DC.