Pollination

General Ecology | Pollination

and changes in plant functional types have been shown experimentally to displace mosses and lichens that are now major components of Arctic vegetation. In Antarctica, warming has caused major regional changes in terrestrial and marine ecosystems. The abundances of krill, Adelie, and Emperor penguins and Weddell seals have declined but the abundances of the only two native higher plants has increased. On continental Antarctica, climate change is affecting the vegetation composed of algae, lichens, and mosses. Introductions of alien species, facilitated by increased warming and increased human activity, are particular threats to southern ecosystems. Recent studies on sub-Antarctic islands have shown increases in the abundance of alien species and negative impacts on the local biota. In contrast, cooling has caused clear local impacts in the Dry Valleys where a 6–9% reduction in lake primary production and a 10% per year decline in soil invertebrates has occurred. The responses of polar environments to climatic warming include feedbacks to the global climate system and other global impacts. Increased runoff from arctic rivers could affect the thermohaline circulation that redistributes the Earth’s heat, thereby causing cooling in the North Atlantic and further warming in the tropics. Reductions in sea ice extent and snow cover together with a shift in vegetation from tundra to shrubs or forests are likely to reduce albedo (reflectivity of the surface) and lead to further warming despite the increased uptake of carbon dioxide by a more productive vegetation. Thawing permafrost is likely to release methane, a parti-

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cularly powerful greenhouse gas, and evidence of this is already available from various arctic areas. Not all impacts of climate warming in polar regions are disadvantageous to society: the reduction of sea ice in the Arctic is likely to lead to increased marine access to resources and new fisheries and reduced length of sea routes, while warming on land will probably lead to increased productivity and increased potential for forestry and agriculture. See also: Alpine Ecosystems and the High-Elevation Treeline; Biological Wastewater Treatment Systems.

Further Reading Anisimor OA, Vaughan DG, Callaghan TV, et al. (2007) Polar regions (Arctic and Antarctic). In: Parry ML, Canziani OF, Palutikof JP, Hanson CE, and Van der Linder PJ (eds.) Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, pp. 655–685. Cambridge: Cambridge University Press. Callaghan TV, Bjo¨rn LO, Chapin FS, III, et al. (2005) Tundra and polar desert ecosystems. In: ACIA. Arctic Climate Impacts Assessment, pp. 243–352. Cambridge: Cambridge University Press. Chapin FS, III, Berman M, Callaghan TV, et al. (2005) Polar ecosystems. In: Hassan R, Scholes R, and Ash N (eds.) Ecosystems and Human Well-Being: Current State and Trends, vol. 1, pp. 719–743. Washington, DC: Island Press. Convey P (2001) Antarctic ecosystems. In: Levin SA (ed.) Encyclopaedia of Biodiversity, vol. 1, pp. 171–184. San Diego: Academic Press. Nutall M and Callaghan TV (2000) The Arctic: Environment, People, Policy, 647pp. Reading: Harwood Academic Publishers. Richter-Menge J, Overland J, Hanna E, et al. (2007) State of the Arctic Report. Walther GR, Post E, Convey P, et al. (2002) Ecological responses to recent climate change. Nature 416(6879): 389–395.

Pollination E Pacini, Universita` di Siena, Siena, Italy ª 2008 Elsevier B.V. All rights reserved.

Introduction and Definitions Pollination from an Evolutionary Point of View Preparing for Dispersal Pollen Presentation and Dispersal Mechanisms

Factors Affecting Pollen Exposure, Dispersal, and Success Further Reading

Introduction and Definitions

and seed development. Irrespective of systematic group, pollination is always affected by biotic and abiotic factors (Table 1). Pollen presentation is the manner in which pollen is presented for dispersal. Pollen may be dispersed as single grains, as in many plants relying on wind dispersal, or in

Pollen is the male gametophyte of gymnosperms and angiosperms. Its size ranges from 15 to 200 mm. Pollination is transport of pollen from its site of production to the female landing site. If successful, it is followed by fertilization

2858 General Ecology | Pollination Table 1 Effects of the main climatic parameters on pollination Temperature

Rain and mist

High T damages flowers and pollen during presentation or dispersal Moderate T facilitates flower and anther opening Low T slows pollen ripening and flower opening and reduces pollinator activity Purge pollen from air, especially at low T Slow flower opening and anther-pollen dehydration May inappropriately rehydrate and reactivate pollen Hinder small animal movements

Sky brightness

Brightness facilitates diurnal pollinator flight Dullness hinders diurnal pollinator flight

Air currents

Facilitate pollen removal and dispersal in anemophilous species Facilitate flower opening and anther dehydration High wind speeds hinder pollinator flight

Pressure variations

Ascending air currents facilitate long-distance pollen dispersal Descending air currents facilitate pollen fallout

groups of grains, as in almost all zoophilous species. Pollen grains may be held together by: 1. common walls, as in tetrads where grains derived from the same meiotic division stay together, or multiple tetrads which may number up to several thousand, as in orchids; 2. threads on the pollen surface or derived from the anther; and

3. viscous fluids, of which pollenkitt is the most common, which also have other functions, such as to keep pollen in the anther until dispersal, to stick pollen to pollinators, to make pollen attractive through scent or color, and to hide or expose pollen to insect sight. Pollen dispersal in clumps is typical of angiosperms. Gymnosperm pollen is produced by pollen sacs in male cones. It is transported by air currents to the ovule micropyle. Angiosperm pollen is produced by anthers of flowers. It is carried to stigmas by animals, air currents, and sometimes water (Table 2). At the end of its flight, pollen may land on female parts of the same or another species, giving rise to legitimate and illegitimate pollination, respectively (Figure 1). Pollen has two walls and when accepted by the female part, emits a tube leading the male gametes toward the female ones inside the ovule. Possible crosses in angiosperms depend on the sexual expression of the plant and on pollen vectors (Figure 1).

Pollination from an Evolutionary Point of View Gymnosperm pollination is invariably anemophilous (primary); only recently evolved genera as Ephedra and Welwitschia are pollinated by insects. There is general agreement that early angiosperms were pollinated by Coleoptera and Diptera. Woody and herbaceous secondary anemophilous angiosperms may descend from zoophilous species. Hydrophily is probably derived from

Table 2 Features of major pollen vectors. Honeybees are the best pollinators because they visit flowers of a given species for as long as they are available, and store pollen for their progeny, unlike nonsocial insects

Pollen vectors Animals

Insects

Honeybees Solitary bees and wasps Flies Butterflies and moths Coleopterab

Specificity (with respect to a flower attractant)

Efficiency

Distancesa (minimum and maximum)

Very high High

Very high High

Several cm ! few hundred m Several cm ! few hundred m

Low Lowd

Moderate Lowd

Several cm ! few hundred m Several cm ! few hundred m

Low Moderate

Several cm ! few hundred m Few m ! few hundred m Several cm ! few hundred m

a

Flying animals and small marsupials

Low

Low Moderate– high Low

Air currents

Breezes Strong winds

Lowe Very low

Low Very low

Few cm ! few hundred m Few hundred m ! several km

Water

Saltc Fresh

Very low Very low

Very low Very low

Some m ! several hundred m Few dm ! several hundred m

Birds

a

Biotic and abiotic environmental parameters may radically affect efficiency and distance traveled. Coleoptera are not good pollinators because they have few hairs and their chewing mouthparts damage flowers. c Underwater pollination occurs in all seaweeds. d Efficiency is low because these animals feed only on nectar and must visit different species in order to have a balanced diet. e Specificity is low but species with this pollination syndrome often grow close to each other, as in the case of grasses and tress. b

General Ecology | Pollination b

a

d

c

H

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pollinator, but pollen attaches to different parts of the pollinator body, so that useless pollination is avoided. Anemophilous species of Juniperus growing in the same environments disperse pollen in different periods.

Preparing for Dispersal b

c

d

M

c

d

D

Figure 1 Scheme of hermaphrodite and unisexual flowers and possible crosses in angiosperms according to plant sexual expression H ¼ plant with hermaphrodite flowers; M ¼ monoecious plant with flowers of both sexes; D ¼ dioecious plant with male and female flowers on different plants. Two plants of the same and one of another species are shown for each type of sexual expression. a ¼ autogamy, b ¼ geitonogamy, and c ¼ heterogamy are legitimate pollination styles though they imply different genetic reassortment; d ¼ xenogamy is illegitimate pollination and gives rise to hybrids in the absence of barriers. Plants with hermaphrodite flowers have all possible crosses; these reduce progressively in monoecious and dioecious plants. Pollen vectors determine pollen cross types. Air and water currents are agents of all types of crosses. Social bees are commonly responsible for a, b, and c, rarely d. Butterflies and moths are most often agents of d, because they only feed on nectar and must visit different flowers to have a balanced diet.

anemophily. Hydrophilous pollen of seagrasses characterized by submarine pollination is 2–3 mm long and a few dozen microns wide. The genus Callitriche has terrestrial, amphibious, and submerged freshwater species; their pollen is spherical and that of submerged species is devoid of exine, as in all species with submarine pollination. Competition to attract pollinators is high when many entomophilous species bloom at the same time and pollinators are few. This is avoided by different blooming periods and anemophily. Examples of entomophilous families with anemophilous members are: Ranunculaceae, Thalictrum; Euphorbiaceae, Mercurialis and castor bean (Ricinus); Asteraceae, ragweed (Ambrosia) and Artemisia. Few entomophilous species bloom at the same time in January and February in Northern Hemisphere Mediterranean environments, when few insects are active. Helleborus bocconei and H. foetidus grow in similar environments and share the same

A fluid fills the anther cavity in which pollen develops. It disappears by evaporation and/or resorption when pollen is ripe, prior to pollen dispersal. Pollen sacs, anthers, and pollen also lose some water. Pollen could be damaged if it were released with a high water content and high metabolic activity. In order to avoid this possibility, pollen is dispersed in a quiescent state, in which cell division and metabolism are arrested. Two classes of pollen, with different levels of developmental arrest, are determined on the basis of their water content at dispersal: partially dehydrated pollen (PDP) has a water content of less than 30% and partially hydrated pollen (PHP) has a water content of more than 30%. The former has metabolic devices to keep its low water content constant; the latter does not have devices and loses water quickly, especially in dry environments. PDP and PHP may be transported by animals or air currents. Both have advantages and disadvantages as well as devices to ensure successful pollination. PDP survives longer at low relative humidity, whereas PHP dries out readily and dies. However, the latter germinates quickly, taking only a few minutes after landing on a stigma. PDP is more common in dry temperate environments and is dispersed during the dry hours of the day. PHP is more common in the Tropics and wet environments; in temperate regions, it is presented for dispersal when RH is high, such as at night or in winter and autumn. Species belonging to these two groups have physiological and ecological strategies to ensure safe pollination journeys, which are quick and short in the case of PHP.

Pollen Presentation and Dispersal Mechanisms When the anther opens, pollen is presented for dispersal and may (1) be launched from the anther by ballistic movements of the anther or stamen and dispersed by air currents, as in Parietaria and castor bean (Ricinus communis); (2) be scattered from the anther by flower movements caused by an insect in search of nectar, and loaded on insect hairs as in Spartium junceum and other Phaseolaceae; (3) be dropped by the anther for lack of any forces to keep it attached, as in grasses and many herbaceous and woody anemophilous species; (4) remain stuck to the anther by pollenkitt or other sticky fluids or threads, pending removal by animals or air currents; (5) be kept in anthers having only small apertures, being released in small doses when the flower is

2860 General Ecology | Pollination

shaken by animals or breezes, as in tomato (Solanum lycopersicum) and Ericaceae; and (6) be dislodged from the anther and presented in another part of the flower (secondary presentation), when flowers are small and disposed in inflorescences where there is no space to expose pollen in the anther, as in daisies such as Bellis. Pollen may be presented for different lengths of time: for zero time, when it is launched, leaving the anther when it opens, as in many anemophilous species having PHP; for a few hours to a month, as in many entomophilous species having PDP; for longer, in the case of orchids. Pollen presentation ceases when the flower closes, as in some species with PHP, probably to avoid dispersal of unviable pollen, or when the anthers are discarded. Animals are attracted to flowers by the prospect of rewards or shelter, or by misleading messages (deception). Common rewards include pollen and nectar, both rich in nutrients: the former contains more proteins whereas the latter contains more carbohydrates. Pollen is collected actively by animals that feed on it and/or passively by those collecting nectar. Each visit to a flower is associated with pollen uptake and discharge.

Factors Affecting Pollen Exposure, Dispersal, and Success The timing for anther opening and pollen release varies with geographical area and season. There are few reports of anthers closing when the weather is wet or during rain. Many flowers open when insects start to fly. In an anemophilous temperate-zone species such as Mercurialis annua, that blooms all year around, anthers open around 7 a.m. in summer and 11–12 a.m. in winter. In temperate zones, anthers of anemophilous and entomophilous flowers generally open from 8 a.m. to 2 p.m., night pollination is restricted to dry summer periods, and night mists purge the air of pollen. In tropical countries, pollination occurs

around the clock, but night pollination is always zoophilous. In temperate countries, pollen vectors vary with the seasons, anemophilous trees pollinating in late autumn and late winter–early spring, when many have shed their leaves. The period when entomophilous pollination may occur progressively reduces from the tropics to the poles. Table 1 shows the main environmental parameters affecting pollination. Pollen may have different probabilities of effecting legitimate pollination (Figure 1), depending on the dispersing vector, and the distances it may travel vary (Table 2). Pollen vectors have different specificities, that is, possibility of transporting pollen to the right landing site. Table 2 shows the specificity, efficiency, and distances reached with different pollination vectors. The main features of anemophilous and entomophilous pollination are shown in Table 3. Abiotic pollination appears random since there are no mechanisms to ensure cross-pollination. Pollen is released into air or water, the movements of which disperse and transport it. When air or water speed is high, pollen may be dispersed long distances, to places where no individuals of the species grow. The further the pollen is dispersed, the less its chance of finding the right female counterpart. Pollen flight is quick and short in farmed anemophilous species, such as wheat, oats, rice, and corn, all of which have PHP. Although anemophily may seem random, in some gymnosperms and angiosperms at least, anemphilous pollen dispersal ceases being random when pollen grains approach the tip of a cone or flower. By virtue of the shape of the grains and female parts, pollen is conveyed by air currents to the right landing site. Pollen lands on the stigma by gravity (anemophily), or because a pollen-dusted insect incidentally touches the stigma. Electrostatic forces are invoked to explain pollen uptake by insects and release on the stigma. Biotic pollination first occurred when an animal touched an anther and incidentally delivered pollen to the female

Table 3 Features of common pollination syndromes Features

Entomophily

Anemophily

Habitus Environment and season Inflorescence Flowers

Isolated herbs, shrubs, and trees Tropical, all year around Temperate, only spring and summer Different types or solitary flowers Hemaphrodite, rarely monoecious or dioecious Large Stamen and stigma often inside corolla

Trees and social herbs such as grasses Tropical, only dry periods Temperate, mainly late autumn and late winter Often pendulous and monoecious Monoecious, dioecious, rarely hermaphrodite

Pollen

Ovules/ovary

With abundant ornamentation With pollenkitt or devices for mass transport Generally many

Inconspicuous, not attractive Pendulous stamen with long filaments and stigma often outside corolla With reduced ornamentation Free, independent grains Generally one

Ecological Indicators | Pollution Indices

counterpart. Interactions between partners began in this way, sometimes leading to species-specific relationships, which are dangerous because if the pollinator becomes extinct or rarefied, the plant can no longer reproduce sexually and will die out if unable to reproduce vegetatively. While pollination is important for plants, being one of the first steps of plant sexual reproduction, for the animal counterpart it represents a source of food: pollen and/or nectar. Abiotic pollination is less expensive for plants because investment in rewards is not necessary; however, investment in an excess of pollen is necessary for random dispersal. See also: Life Forms, Plants; Plant Growth Models; Plant Ecology; Seed Dispersal.

Further Reading Ackerman JD (2000) Abiotic pollen and pollination: Ecological, functional, and evolutionary perspectives. Plant Systematics and Evolution 222: 167–185.

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Cooper RL, Osborn JM, and Philbrick CT (2000) Comparative morphology and ultrastructure of the Callitrichaceae. American Journal of Botany 87: 161–175. Dafni A, Kevan PG, and Husband C (2005) Practical Pollination Biology. Cambridge, ON: Enviroquest. Gelbart G and von Aderkas P (2002) Ovular secretions as part of pollination mechanism in conifers. Annals of Forest Science 59: 345–357. Linder HP and Midgley J (1996) Anemophilous plants select pollen from their own species from the air. Oecologia 108: 85–87. Lindgren D, Paule L, Xihuan S, et al. (1995) Can viable pollen carry Scots pine genes over long distances? Grana 34: 64–69. Nepi M, Franchi GG, and Pacini E (2001) Pollen hydration status at dispersal: Cytophysiological features and strategies. Protoplasma 216: 171–180. Pacini E (2000) From anther and pollen ripening to pollen presentation. Plant Systematics and Evolution 222: 19–43. Pacini E and Hesse M (2005) Pollenkitt – Its composition, forms and function. Flora 200: 399–415. Thien LB, Azuma H, and Kawano S (2000) New perspective on the pollination biology of basal angiosperms. International Journal of Plant Sciences 161(supplement 6): S225–S235. Vaknin Y, Gan-mor S, Bechar A, Ronen B, and Eisikowithch D (2001) Are flowers morphologically adapted to take advantage of electrostatic forces in pollination? New Phytologist 152: 301–306.

Pollution Indices G Bellan, Centre d’Oce´anologie de Marseille, Marseilles, France ª 2008 Elsevier B.V. All rights reserved.

Introduction Biological Indicators: A Recall

Conclusion Further Reading

Introduction

is usually considered as the quality of state of resources in relation to human use. This anthropomorphic approach consists in measuring the environmental variables that could define, ‘objectively’, the characteristics of a supposed state of quality or of resources directly and profitably used by humans. It needs to be remembered that policies for management of land, fresh and marine waters tend to maintain minimum levels of acceptable quality permitting to protect the health of populations and their possibility to benefit or utilize their environment without major problems. This ‘physical–chemical’ approach only can ensure the quality of environment and the preservation of its resources over the short run, within the framework of given place, time, and aims. It is not able to take into account whether or not the quality of resources would meet fundamental needs of the environment as a whole. The interpretation of such a quality in terms of protection of environment should be integrated, providing that the use of resources and environment preserves effectively high levels of quality of life, not restricted to humans.

This article presents pollution indices in the following perspectives: in a biological (sensu lato) perspective applied to the ecological indicators; and in the framework of ecology applied to the protection and management of the environment. The quality of the environment could be monitored according to two complementary approaches: the detection of pollutants or any other materials naturally or artificially introduced in the environment; and the evaluation of the effects of these pollutants or materials on living organisms, even at the level of individuals or at higher levels, that is, populations and communities (Figure 1). Traditionally, physical state and chemical state or their combinations are usually employed as testimony of the state of environment, mainly as the overall degree of pollution (or absence of pollution) of a more specific environment (water, air, soil, etc.). These categories of indicators are based upon the fact that environment quality