The origin and rarity of botanical carnivory

TREE vol. 2, no. 12, December 1987

The Origin Carnivory David H, Benzing

and Rarity of Botanical

Most plants are strict producers: they create the biomass consumed by animals and other heterotrophs to sustain life. Occasionally, the tables are turned and the plant becomes predator and the animal prey. Botanical carnivores remind us that some vascular plants have evolved remarkable mechanisms for acquiring hey nutrients. Likewise, they demonstrate the parallels between disparate fife forms and show how evolution has rearranged ex- isting characters into novel combinations to achieve new functions. But despite its obvious advantages and substantial geological history, botanical carnivory remains a minor nutritional mode, apparently because prey use is usually not the most economical way for plants to secure nutrients.

The animal-like qualities of carnivorous plants have spawned in- ordinate interest, not least among several of the most eminent natural historians. Charles Darwin’s mono- graph’ on these remarkable organisms is especially discerning and represents a clear departure from some of the fanciful speculations offered by his contemporaries. De- spite Darwin’s enlightened views and firm corroboration since, however, many still view botanical carnivores and nitrogen-autotrophic (non-carnivorous) vegetation as fundamentally distinct. Actually, normal encounters that occur between all higher plants and animals share some rather basic characteristics; these common attributes and the uncommon occurrence of botanical carnivory provide focus for this review.

Systematic occurrence and mechanisms of camivoty

Carnivorousvascularplantsattract, trap, kill and digest captured prey, ultimately absorbing and trans- locating the nutritive yield2e3. All but Brocchinia (perhaps two species) and Catopsis berteroniana of the Bromeliaceae are dicots; at least seven families of Magnoliopsida, all relatively small (Table 11, contain

David Benzing is at the Dept of Biology, Oberlin College, 103 Kettering Science Building, OH 44074, USA.

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prey-utilizing members. Predatory plants share other traits: undimin- ished dependence on photosynthesis and occurrence in wet or seasonally humid, well-exposed habitats with nutrient-poor soils. Supplemental phosphorus (PI and nitrogen (N), probably in different order depending on the habitat, are the most significant rewards of botanical camivory@. Other elements must be important too7, but carbon derived from prey is not; carnivorous plants cannot sur- vive in darkness even if provided with supplements from captured animals. Well-exposed specimens

will mature without access to carcasses but, denied abundant nutrients from other sources, flower- ing and vegetative vigor are diminished5f8e9.

Capture is effected through various contrivances (Fig. I 1, some pas- sive and others more dynamic (Table I). Food processing depends on symbionts (as in some pitcher plants and the bromeli- adslo) or on enzymes secreted from tank leaves, adhesive foliage or ac- tive traps. Attraction may involve color, including UV reflectance”, and (in some pitfall carnivores) nectar and odor as well. The type of enticement can determine the most important food source: ants for Brocchinia and Heliamphora; small flying insects for many Drosera; plankton for Utricularia.

zig. I. Representative carnivorous plants illustrating habits and a variety of devices for prey rse. A, Sarracenia purpurea; B, Cenlisea sp.; C. Brocchinia reducta; D, L/trim/aria inf/ata; E. 2rosera rotundifolia; F, Dionaea muscipula.

@ ,987 Eisewer Publications Cambrld9e 0169 5347’87~$02 00


Table I. Families and genera of the conventionally recognized carnivorous plants, thelr approximate numbers of species, world-wide distribution, capturing mechanisms (adapted from luniperiV and evidence of extended geologkal age

_

Family, genus No. of Geographic Capturing mechanism Fossils and other evidence of species distribution suction snap pitfall adhesive extended geological age

trap trap trap trap

Sarraceniaceae Heliamphora 3+ Venezuela, Guiana, Brazil + Relic distributions on ancient Sarracenia 9? Eastern N America + sediments (Heliamphoraj Darlingtonia 1 Northern California, +

southern Oregon Nepenthaceae

Nepenthes 90+ Eastern tropics, west- + ward to Ceylon, the Seychelles, Madagascar

Droseraceae Dionaea 1 N and S Carolina Upper Cretaceous seeds Aldrovanda 1 Ubiquitous (Aldrovanda)28; Drosoph yllum 1 Portugal, Spain, Morocco + Eocene pollen (Aldrovanda, Drosera 90+ Ubiquitous, but approx. + Drosera) 2s;

half of spp. in relic distribution (Dionaea); SW Australia world-wide distribution

despite limited dispersibility (Aldrovanda, Drosera)

Dioncophyllaceae Triphyophyhum 1 Sierra Leone, Liberia, + Eocene seeds (relative of

S W Ivory Coast Triph yoph y//urn)29 Byblidaceae

B yblis 2 N W to S W Australia + Relic distributions on ancient sediments

Cephalotaceae Cephalotus 1 Extreme S W Australia Relic distributions on ancient

sediments Lentibulariaceae

Pinguicula 30+ N and S hemispheres + World-wide distribution Utricularia 250+ Ubiquitous + despite limited dispersibility Biovularia 2 One species in Brazil, + (GenIisea, Pinguicula,

one in Australia Utricularia) Polypompholyx 2+ Tropical Australia and +

S America Genlisea 12 Brazil, Guianas, Cuba, +

W Africa Bromeliaceae

Brocchinia reducta 1 S E Venezuela and + Relic distributions on ancient Guianas sediments (Brocchinia)18

Catopsis berteroniana 1 S Florida to S E Brazil +

Minor differences in habit and location may lead to resource partitioning between taxa: two co- occurring Drosera species in Ger- many feed primarily on Collembola or winged prey respectivelyr2. Modification for prey use is not incompatible with conventional carbon gain, and most traps retain some green tissue.

History and similarity to N-autotrophic plants

There is no clear picture of how often, by what route, or when carnivory emerged during plant evolution. Neither fossils nor extant taxa reveal transitions from N- autotrophy, but prey use is ancient (Table I). Glands provide the best example of shifting functions; for instance, nectaries located at the orifices of certain Sarracenia leaves grade into digestive glands lining trap surfaces belowr3fr4. Little fun- damental change may have been

necessary because the mechanisms for biosynthesis and secretion are similar whether the product is nectar, mucilage or a solution of hydrolytic proteinsr5. Moreover, structural antecedents of glands involved in prey use are universal if the smaller of the two types of secretory-absorptive appendages in Cephalotus are indeed modified stomatarb. Glandular products required for prey immobilization and processing have other functions elsewhere, as do numerous other characters associated with carnivory (Table 2). Botanical carnivory is unique only for the ways in which widely available characteristics have been enhanced and com- bined to create the varied syndromes that effect prey use13e14.

Phylogenetic constraints and predispositions for botanical camivory

Themes such as salt tolerance in Chenopodiaceae, epiphytism in

Orchidaceae, ruderalism in Bras- sicaceae, and (less consistently) carnivory in Bromeliaceae, Scro- phulariales and the other major taxa harboring prey-dependent species, characterize many angio- spermous groups. This illustrates that (I) some evolutionary outcomes were more likely in some lineages than in others, and (2) not all of these potential outcomes were possible for all lineages. Prop- erties that reduce the capacity to respond to directional selection, or what are called ‘phylogenetic’ or ‘design’ constraints, always influence radiation. In effect, evolutionary innovations require appropriate ancestral form and function, or more specifically, existence of the genetic foundation responsible for those traits. Moreover, inherent resistance to adoption of a particular capacity like camivory is to some degree inversely related to potential benefit; phylogenetic

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Table 2. Characters involved in the carnivorous syndrome and their functions elsewhere

Character Function in N-autotrophic taxa and in activities of carnivores unrelated to prey use

Nectar: Aids prey capture in numerous pitcher plants, Brocchinia reducta18

Anthocyanins: Abundant in traps of many carnivores

Odor:

Attraction of pollinators or pugnacious ants

Attraction of pollinators and seed dispersers, sun screening

Aids prey capture in some pitcher plants, Attraction of pollinators and seed Brocchinia reducta18 dispersers

Epicuticular’waxes: Loose flakes lubricate traps and prevent Sun screening, waterproofing, defense prey escape in Catopsis berteroniana, against climbing predators and Brocchinia reducta, and Nepenthes13,18-24 pathogens13,14

External mucilage: Aids prey capture in Drosera, Dionaea, Pinguicula and others

Lytic enzymes: Promote prey digestion for most carnivores

Glandular hairs: Part of the trapping/digesting complex of Triphyophyllum, Byblis and others

Absorptive hairs:

Lubrication of root-tip growth, moisture retention and accumulation, defense

Cell metabolism (those of Dionaea similar to lysosome contentsJ30

Trap (e.g. Nicotiana, Silene) and/or kill (e.g. Stylosanthes) predators; salt and nectar secretion13,14,16

Line traps of Brocchinia reducta, Dionaea Water and nutrient ion absorption and many others (e.g. Bromeliaceae)24

Stimulated motor responses followed by rapid acid growth: Aid prey capture in Dionaea31-32 and Movement of sexual parts (e.g. Berberis probably other carnivores with snap traps stamens, Mimulus stigma), leaf closure

(e.g. Mimosa pulvinus) Animal capture (all carnivores) Temporary retention of pollinators (e.g.

aroid inflorescence, orchid flowers)J3.‘4 Phytotelmata:

These water-containing plant cavities permit prey capture and processing in pitcher plants and carnivorous bromeliads

Water and nutrient source (e.g. tank bromeliads)24

Nutrient absorption through shoot surface Generally operative in tracheophytes but (all carnivores): especially well developed in various

epiphyte9, myrmecophytes33and aquatic macrophytes

constraints can be overcome if selective pressure is strong enough - that is, if the resulting advantage is sufficiently great.

Such obvious accommodations to ancestral growing conditions as particular modes of resource utilization, defensive killing and pol- linator attraction favored the emergence of N-heterotrophy’3n14. Nitrogen must have been particularly important in the evolutionary process. Acquisition and use of N is complex; supplies vary in quantity and kind with habitat, and costs differ. Processing sites (roots versus shoots) and associated problems of pH and ion regulation render some N-containing molecules more suit- able than others, depending on metabolic competence, habit and the environmental contextl7. Users of Nz and NH4+, for instance, must eliminate excess protons; N03- assimilators consume or excrete ex-

cess OH-. Although the NH4+-to- protein pathway is less expensive in terms of direct energy consump- tion, other sources may be superior even where NH4+ is in greatest supply. Soil is the usual sink for excess H+; indeed, owing to the phloem-immobile nature of protons, terrestrial plants process most acquired NH4+ in roots - a potential problem for botanical carnivores and other taxa with diminished root systems.

Few recognized carnivorous characters concern metabolism of absorbed N or disposal of poten- tially problematic by-products. Rather, they involve conspicuous features like glandular trichomes, rapid growth responses, lytic secretions, colors and appropriate leaf forms. Mechanisms that lure, capture and process prey have been shuffled into various arrange- ments for different purposes in car-

nivorous and N-autotrophic plants alike (Tables I and 2; Fig. I). Genes coding for these versatile characters are far more widespread in Magnoliophyta than is carnivory itself, apparently because some additional requisite that permits use of organic N derived from prey is also uncommon.

Appreciation of the superficiality and interchangeability of the more obvious components of carnivorous syndromes and their possible ori- gins is increased by considering related N-heterotrophic lineages and the overall rarity of animal use for food. Species belonging to Len- tibulariaceae (Table IL for instance, secure prey with simple adhesive leaves (Pinguicula) and ultra- sophisticated suction-traps (Utricu- lark sensu l&o; Fig. 1 J; GenIisea produces a unique, remarkably complex spiral appendage. Various evolutionary pathways could have led to this constellation of carnivorous taxa. Among the possibilities are ( 1 I the three genera in Lentibu- lariaceae may be parallel deriva- tives from one N-autotrophic ancestor that was predisposed for prey use; (2) the distinct kinds of trap employed in this family may illustrate stages in a phylogenetic sequence much like that proposed by JuniperI for Droseraceae (Fig. 2); (3) the modern genera of Len- tibulariaceae could have arisen independently from a lineage em- bodying a very generalized cami- vorous syndrome.

The first option assumes that a propensity for botanical carnivory existed and included factors that were less widespread than was access to a particular set of ancillary characters concerned with acquiring and digesting prey. The other two options imply that the more specialized carnivorous syndromes were derived from fewer, less complex modes of prey utilization. The apparent strength and pervasive- ness of phylogenetic constraints on the emergence of prey use in Mag- noliophyta - i.e. the number of times this capacity arose de novo in distantly-related lineages - depends on which of these routes was the most important during the evolution of botanical carnivory. The history of carnivory will be clearer when factors affecting the cost of metabolizing key nutrients,

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relationships among carnivorous species, and the homology of characters involved in their unusual nutrition, become better known. A look at the overall economics of prey use is equally important to these questions and to related problems concerning the existence of predisposing metabolic foun- dations and why botanical carnivores are so few.

Resource economy, plant performance and the occurrence of botanical carnivory

The ability of plants to counter the resource scarcity that limits photosynthesis varies widely. Mechan- isms for obtaining and using water economically for production of biomass on land are widely available, but access to critical nutrient ions is another matter. Only a small pro- portion of the most concentrated sources of chemically available N and P (i.e. xylem and phloem sap and animal bodies) is utilized by botanical parasites and carnivores, and by trophic ant plants. Most tracheophytes draw mineral ions primarily from soil where nutrients are often scarce. Similarly, xero- phytes are numerous, taxonomic- ally diverse, and dominate vast land areas while plants that tap the abundant ion supply in animal carcasses number less than 500 species (~0.5% of the total; Table 1). Moreover, carnivorous species almost never dominate communities, despite a worldwide distribution that reveals tolerance for a variety of regional climates and many substrata.

Givnish et aI.’ have developed a model that addresses this paradox by demonstrating that botanical carnivory is probably no more than marginally successful even where it is most efficacious. This model was offered primarily to illustrate the generally unfavorable energetics and thus impracticality of prey use, but it also provides perspective on the question of why some lineages rather than others have evolved N-heterotrophy.

Plant success in a particular en- vironment ultimately requires a proscribed fecundity, a parameter intimately tied to carbon/energy balance and thereby coupled to supplies of water, radiant energy and nutritive elements, particularly N and P. Scarcity of any one of

A D”OIEll

C DIO*OP”“Lt_“M D DROIFRA E DlONIEI

Fig. 2. Putative homologies between structures involved in prey use in Droseraceae13,‘*. A-B: Derivation of Dionaea trap from tentacled Drosera leaf. C-E: Sequence leading from individual tentacle of Drosophyllum to trigger hair of Dionaea. Reproduced, witlr permission, from Refs I4 and 34.

these resources diminishes fitness by reducing photosynthesis, a fact that helps to explain why carnivorous plants only occur in certain habitats and why botanical carnivory ranks as a minor rather than a globally significant nutritional mechanism. Because prey use ex- ists primarily to ensure adequate supplies of mineral nutrients, this mechanism has to be compatible with the ways in which all of the other required resources are pro- cured and usedr9. Plant growth is governed by tradeoffs which ensure that the more abundant resources are deployed so as to mitigate shortages of the least plentiful ones in order to optimize overall performance. In essence, resource allocation during ontogeny is tailored so that the impact of scarcity is minimized and excess plant capacity is simultaneously avoided.

The process operates at several levels of biological organization. A

community of desert plants, for instance, never harvests as much of the available photons as of the available moisture. Root systems ramify extensively through the arid soil whereas the collective canopy they support is much less con- tinuous. Increase in the relatively sparse leaf area in order to inter- cept more light would necessitate diminished investment in roots and not only create unusable capacity for photoassimilation but heighten vulnerability to drought, At the level of the single leaf produced in shade rather than in full exposure, more N is invested in light- harvesting machinery than in car- boxylating enzymes because photons under a dense canopy limit photosynthesis more than does the supply of C02. Conversely, sun leaves contain proportionally greater investment in dark-reaction machinery.

According to Givnish et a1.18, prey utilization enhances carbon gain


D E

Fig. 3. Representative trophic mynnecophytes illustrating habits and a variety of nesting sites. A, Tilland- sia bulbosa; B, Schlumbergia sp.; C, Hydnophytom formicarium; D, Lecanopteris carnosa; E, Dischidia rafflesiana.

relative to that possible for co- occurring N-autotrophic plants by two mechanisms: increase in a leaf’s photosynthetic capacity via N-enrichment per unit of leaf area, and production of more foliage. There is positive correspondence between maximum potential photosynthesis (A,,,) and N content of leaves20 but, as Givnish et al. noted, supplementing soil-derived N via carnivory incurs extraordinary cost; traps and related secretions, like any other plant product, repre- sent transformed photosynthate.

Abundance of photons and moisture

Fig. 4. A graphic model illustrating how aspects of resource supply and economy influence the ecological occurrence of carnivorous plants. See text for details.

Although animal-capturing leaves remain green, direct energy returns on investment are greater from organs designed primarily for carbon gain. Of course, costs for enzymes, lubricants and odors that yield no direct returns at all can be high. Pate* i estimated that secretions from the tentacles of a Drosera consume 4-6% of the plant’s total carbon budget, a figure not unlike that proposed for the maintenance of mycorrhizas and the cost of N2 fixation by some legumes.

Investment in carnivory will yield returns that exceed cost only when greater photosynthetic capacity is generated than would be possible without that input. Habitat quality will ultimately determine cost effectiveness. Should a site be sufficiently fertile, there is no impetus to sacrifice photosynthate for non- productive components of a carnivorous syndrome, or to diminish autotrophic function through dual use of foliage for mineral ion and carbon-energy gainIs. Conjecture based on economic considerations was offered to explain the almost complete restriction of ant-fed plants to epiphytic habitats22. Trophic myrmecophily, like botanical carnivory, arose about six timesl3, as indicated by the disparate taxa and diverse accommoda- tion for ant colonies involved (Fig. 3). Additional fitness gained from investment in nesting sites and food rewards by these ant- inhabited plants depends on whether resident insects provide defense as well as nutrients. Other determinants of cost effectiveness are the abundance of founding queens and the number and quality of alternative nesting oppor- tunities.

Environmental factors apart from nutrient scarcity also set the value on botanical carnivory. Should drought or shade, more than nutrient insufficiency, curtail photosynthesis, selection will encourage habits and physiologies favoring acquisition and efficient use of light or moisture rather than promotion of access to nutrient supplements in prey. Allocation patterns evolved in dark habitats would be biased toward production of large masses of durable shade-adapted foliage; on arid sites, toward large root

masses and canopies capable of extraordinary water economy.

Figure 4 illustrates under what moisture and light regimens a carnivorous plant would outproduce an otherwise similar N-autotrophic plant. Note that the cost/benefit function representing economy of prey use in fertile habitats as opposed to that on lower-quality sites never rises above the cross- hatched zone within which botanical camivory is unsustainable. Above this zone it is possible, but not to the exclusion of genotypes that also experience lower de- mands for soil nutrients for other reasons (e.g. evergreenness, slow growth). Remember that there are no exclusively carnivorous plant communities. Where substrata are fertile, soil nutrients can be obtained so inexpensively that carnivory is uneconomical and all flora will be N-autotrophic, as indeed is the case in most habitats. Botanical carnivory pays only where scarcity of key nutrients more than shade or drought constrains growth.

Aspects of carnivorous plant biology support the economic model. Many botanical carnivores exhibit seasonal heterophylly by produc- ing leaves without traps or with increased photosynthetic area at times when growth is likely to be limited by factors other than nutrient ion supplyi8. Some Sar- rucenia produce simple phyllodes during late summer droughts. Dionaea and Cephalotus form leaves with diminished or no trapping capacity at all during cool winter months. Tripkyopkyllum produces glandular trichomes on juvenile foliage just before the rainy months commence23. Seasonal changes in resource supplies (including potential prey) and vulnerability associated with year-round maintenance of transpiration-prone traps could also influence these growth patterns. The occurrence of just two or three carnivores among the hun- dreds of phytotelm bromeliads that instead derive nutrients at lower cost from impounded humus18~24~25 also supports the proposal that prey use is unsustainable unless nutrient scarcity is the most important limit to plant vigor.

Conclusions Considering the abundant nutri-

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ents in animal tissue, the apparent ready access to many traits associated with carnivory, and the long history of complete carnivorous syndromes, one wonders whether prey use is not more common than is currently realized. Unequivocally carnivorous species may simply be the most specialized members of a much larger group3. Those plants that trap via sticky secretions (e.g. Nicotiana, Silene, S~lanurn)~~ or kill (e.g. Stylosatithes and the putatively near-carnivore Roridula)‘3 or pos- sess killer seeds (e.g. Capsellu26) yet fail to meet the traditional defini- tion of botanical carnivory, may achieve more modest nutritional gains at lower cost. Benefit could be secondary to defensive killing; usable products from carcasses may simply be absorbed after being washed into the soil. The giant Andean bromeliad Puya rainzondii garners ions from small birds killed by foliar spines27 evolved to deter mammalian her- bivores. But unless cryptic mechanisms of significant nutritional importance are found to be widespread - a rather unlikely prospect - one conclusion is unmistakable: the land flora has not been widely successful in short-circuiting the bio- geochemical cycles of key mineral elements to increase productivity.

Global photosynthesis probably remains more constrained by the activities of decomposers and other consumers (particularly detritivores) than would be the case if prey use were more economical, phylogenetic constraints consequently relaxed, and the diversity of botanical carnivores greater.

References I Darwin, C.R. ( 1875) Insectivorous Plants, John Murray 2 Lloyd, F.E. (19421 The Carnivorous Plants, Dover Publications 3 Heslop-Harrison, Y. (1978) Sci. Am. 238, 729-73 I 4 Luttge, U. ( 1983) in Encyclopedia of Plant Physiology (Vol. 12CI (Lange. O.L. Nobel, P.S., Osmond. C.B. and Ziegler, H., eds), pp. 489-5 17, Springer-Verlag 5 Chandler, G.E. and Anderson, J.W. ( 19761 New Phytol. 76, 129-141 6 Karlsson. P.S. and Carlsson, B. ( 1984) New Phytof. 97,25-30 7 Folkerts, G.W. t 19821 Am. Sci. 70,260-267 8 Pringsheim, E.G. and Pringsheim, 0. ( 1962) Am. J. Bot. 49,898-901 9 Aldenius, I., Carlsson, B. and Karlsson. S. (19831 New Phytof. 93,53-59 IO Bradshaw. W.E. (19831 in Phytotelmata: Terrestrial Plants as Hosts for Aquatic Insect Communities I Frank, 1.H. and Lounibos, L.P., eds), pp. 161-189. Plexus Publishing II Noel, D.M., juniper, B.E. and Dafni, A. (1985) New Phytol. lOl,585-593 I2 Thum,M. tl986)Oecologia 70.601-605 13 juniper, B.E., Robins, R.j. and loel. D.M. The Carnivorous Plants, Academic Press (in press) I4 juniper, B.E. ( 1986) in Insectsand the Plant Surface (luniper, B.E. and Southwood, T.R.E.,

edst, pp. 195-218, Edward Arnold 15 Heslop-Harrison, Y. (I9761 in Perspectives in ExperimentalBiology (Vol. 21, (Sunderland, N., ed.1, pp. 463-476, Pergamon I6 Parkes, D.M.and Hallam. N.D. 11984) Aust I. Bot. 32, 595-604 17 Raven, J.A. (1985) New Phytol. lOl,25-77 18 Givnish. T.I., Burkhardt, E.L.. Happel. R and Weintraub, I. ( 19841 Am. Nat. 124, 479-497 I9 Bloom, A.]., Chapin. F.S. and Mooney, H.A. (1985) Annu. Rev. Ecol. Syst. 16, 363-392 20 Field, C. and Mooney, H.A. (19861 in On the Economy of Plant Form and Function (Civnish, T.I., ed.t, pp. 25-55, Cambridge University Press 21 Pate, IS. 11986) in On the Economy o/Plant Form and Function (Givnish, T.I.. ed.), pp. 299-325, Cambridge University Press 22 Thompson, I.N. f 1981 I Bot. J. Linn. Sot. 16, 147-155 23 Green, S. Green, T.L. and Heslop- Harrison, Y. II9791 Bot. I. Linn. Sot. 78,99-l 16 24 Benzing, D.H., Civnish, T.J. and Bermudes. D. (19851 Syst. Bot. IO, 81-91 25 Benzine. D.H. II9861 in Insects and the Plant Surface (Juniper. B.E. and Southwood, T.R.E.. edsl, pp. 235-256, Edward Arnold 26 Barber, I.T. (1977) Plant Physrol. iSuppl.1 59, 35 (Abstract No. 1931 27 Rees, W.E.and Roe, N.A. (1980) Can. 1. Bot. 58, 1262-l 268 28 Knobloch. E. ( 19871 XIV Internal. Bot. Congress Abstract 5-30-5

29 Muller, I. I1981 I Bot. Rev. 47, l-l 42

30 Robins, R.I. and Juniper, B.E. ( 1980) New Phytol. 86,4 13-422

31 Robins, R.I. ( 1976) Planta 128, 263-265 32 Williams, S.E. and Bennett, A.B. ( I9821 Science 218, Il20-I 124

33 Huxley, C.R. ( 19801 Biol. Rev. 55, 321-340

34 Williams, S.E. ( 19761 Proc Am. Phifos. Sot. I 20, 187-204

Diversity: Cultural and Biological Early human populations utilized a wide range of biological resources in a tremendous diversity of environments. As a result, they possessed high [eve/s of cultural diversity dependent on and supportive of high levels of biological diversity. This pattern changed drastically with technological innovations enabling certain human groups to Greak down territorial barriers and to usurp resources of other groups. The dominant groups have gone on to exhaust a whole range of resources, depleting both biological and cultural diversity. Traditions of resource conservation can, however, re-emerge when the dominant cultures spread over the entire area and the innovations diffuse to other human groups. This could change once again as genetically engineered organisms become an economically via6le proposition with the accruing advantages concentrated in the hands of a few human groups: a further drastic reduction in biological and cultural diversity may ensue.

The diversity of life on earth is a major cause of loss of biological currently under serious threat; so is diversity, there is serious interest the diversity of human cultures. in understanding how the diversity Since the now dominant techno- of human cultures relates to the logical culture is often perceived as conservation of biological diversity,

and whether the attempts to conserve biological and cultural

Madhav Gadgil is at the Centre for Ecological diversity could go hand in hand’.

Sciences, Indian Institute of Science, Bangalore Biological diversity has increased 560012, India. through evolutionary time, presum-

(6 ,987, t~%e\‘Ii~r PilO Ir,>‘I (,i LIIV IU1Ia”e 0169 I>341 87 SO? on

Madhav Gadgil

ably because much of it arises through diversity of adaptations to environmental heterogeneity, which itself has been continually enhanced by the activities of living organismG3. Part of the adaptation of organisms is behavioural, with behaviour becoming increasingly flexible in higher animals. Thus birds and mammals take to new food sources by imitating other members of their social group4. Biologists define culture as such acquisition of behavioural traits from conspecifics through social learning; and man’s close relatives, such as chimpanzees, have pro- gressed further by introducing de- liberate teachings. The capacity for tool use and symbolic communica- tion has, however, enabled the

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The origin and rarity of botanical carnivory