Differential foraging for resources, and structural plasticity in plants

TREE vol. 3, no. 8, August

20 Batzli, G.O., White, R.G., MacLean, Jr, S.F., Pitelka, F.A. and Collier, B.D. ( 19801 in An Arctic Ecosystem: the Co&a/ Tundra at Barrow, Alaska (Brown, f., Miller, P.C.,

Tieszen, L.L.and Bunnell, F.L.. edsl, pp. 335-410, Dowden, Hutchinson and Ross H. (1983) Oikos 21 Laine, K. and Henttonen, 40,407-418 22 Bulmer, M.G. 11974) /. Anim. Eco/. 43, 701-718 23 Danell, K. (1985) Acta Therio/. 30,219-227 24 Buehler, D.A.and Keith, L.B. (19821 Can. Field Nat. 96, 19-29 25 Keith, L.B. (19831 Oikos. 40,385-395 E. and Widen, P. 26 Angelstam, P., Lindstriim,

( I985 I Holarct.

Ecol. 8.285-298

27 HBrnfeldt,

B. (19781 Oecologia (Berlin) 32. 141-152 28 Brummer-Korvenkontio, M., Henttonen, H. and Vaheri, A. ( 19821 Stand. 1. Infect. Dis.

ISuppl. 361,88-91 29 Niklasson. B. and LeDuc,

J ( 198711. Infect. Dis. I55,269-276 30 Kaplan, C., Healing, T.D.. Evans, N.. Healing, L. and Prior, A. ( 198011. Hyg. 84, 285-294 31 Descoteaux. j.P and Mihok. S II9861 1. Wildl. Dis. 22, 3 14-3 I9 32 Henttonen, H.. Oksanen, T lortikka, A and Haukisalmi, V 119871 Oikos 50.353-365 33 Andersson, M. and jonasson, S I I9861 Oikos 46,93- IO6

Michael Hutchings is at the School of Biological Sciences, University of Sussex, Falmer, Brighton, Sussex BN I 9QC, UK.

200

35 Jonasson. S., Bryant, j.P, Chapin Ill, F.S and Andersson, M ( 19861 ,4m. Nat. I28 194-408

I I9861

S Cbransson, C Hansson, L Hbgstedt, G.. Liberg. 0:, Nilsson. I., Nilsson, T von Schantz, T and SylvCn, M. (19831 Oikos 40,X--52

37 Erlinge,

38 Sievert, P R. and Keith, Manage. 49,854-865 39 Danell, Oecologia

Michael J. Hutchings

The term ‘foraging’ can be defined as the process whereby an organism searches or ramifies within its habitat in the activity of acquiring essential resources*. Unless the pattern of search changes when the organism encounters patches of habitat containing different concentrations of resources, however, acquisition of resources will not be achieved efficiently. In plants, changing search patterns are usual-

1V / 19851 Am

36 Lindroth, R.L. and Batzli, C 0 / Anim. Ecol. 55,43 I-449

DifferentialForagingfor Resources andStructuralPlasticityin Plants Although ecologists have spent much effort in analysing the foraging behaviour of animals, the study of plants as foraging organisms is a relatively unexplored subject. There is often, however, much greater potential for analysis of foraging behaviour in plants than in animals. Unlike most animals, many plant species leave permanent or semi-permanent records of their foraging activities because their resourceacquiring structures (primarily leaves and roots), persist for a considerable time, as also do the structures (trunk branches, stolons, runners or rhizomes) which enable leaves or roots to be projected into particular positions in the habitat. In addition, plant ecologists are not burdened with the difficulties associated with determining how changes in foraging behaviour affect fitness in animals’, because plant muss (or, in the case of clonal species, number of ramets produced), is usually closely correlated with fitness.

34 Fowler. S.V. and Lawton, Nat. 126, 181-195

1988

ly achieved through morphological plasticity*“. Interpretations of experimental data on plant form in terms of differential foraging were almost entirely lacking from the ecological literature until recently. For such interpretations to be possible experiments on plants in controlled environments, rather than observations of plant behaviour under field conditions, are essential. This is because the natural environment is highly heterogeneous even at a very small scale; the genetical origin (and therefore the morphological properties) of plants in the field may be uncertain even within a species, and the effects on morphology of interactions the between the plants under study and neighbouring plants are very complex7. Altogether these considerations confound attempts to interpret morphological differences within a species from place to place in the field in terms of differential foraging. Greenhouse experiments on foraging Most references to plants as foraging organisms concern herbaceous clonal species that grow primarily in the horizontal plane, branching and spreading laterally rather than acquiring heighta-lo. Most of the available data about plant foraging are from such species. The behaviour of these species is clearly easier to analyse than C

K. and Hornteldt, 73, 533~-5%

1. B. (I9851 /. Wild/

B. I19871

that of species with markedly three-dimensional growth forms. In the clonal herb Clechoma hederacea (ground ivy t, resource acquisition is primarily carried out by two-leaved structures termed ramets, which are produced at every node along stolons which creep over the soil surface (Fig. I t The plant also produces roots at its nodes. Two further stolons can grow from lateral buds at each node, so that the clone develops as a branched, connected population of ramets. For descriptive purposes. the principal stolons and the ramets they bear are described as primaries, whereas lateral buds give rise to secondary (and tertiary I stolons and ramets. Although the ramets are strictly determinate in form, the whole clone is markedly plastic in structure. Plants of G. hederacea for experimentation can be proliferated from a single clone, so that all observed variation in morphology can be ascribed to differences in the grow-ing conditions applied to replicate clones. Each ramet is large enough. and far enough from its neighbours on the same stolon, to be subjected in experiments to its own personalized set of growing conditions. Thus it could be provided, if wished, with a supply of light, nutrients and water which is different from that given to every other ramet. Experiments have been per” formed to compare the morphology of whole clones given either ample or very limited supplies of either nutrients or light>,“,’ In addition to the expected reduction in biomass ot clones when resource supply was low, there were marked differences in the morphologies of clones receiv-

TREE vol. 3, no. 8, August

1988

(a) ing ample and limited resources. Most of the changes in morphology were qualitatively similar regardless of whether nutrient or light was imited in supply, although under :he conditions of the experiments, ight had a greater effect than nurient availability. The principal :hanges under low resource supply Nere reduced branching, longer nternodes, less weight per unit ength of stolon and a change in the 3roportional allocation of biomass .o different structural components; ,Nhile there were some differences n the way in which this was exlressed under low nutrient and low ight conditions, clones receiving ‘imited supplies of either resource allocated significantly more biomass to stolons than clones given ,rmple resources. Although there were significant differences in the iota1 length of stolons and the total number of ramets produced by c:lones under different conditions, there was no difference in the length of primary stolons produced ,rnd little difference in the number :)f primary ramets (Fig. 2). Using Clegg’s (L. Clegg, PhD “hesis, University of Wales, UK, 9781 terminology, the clones 1:hanged from having relatively ijhalanx morphologies given abunrelatively dant resources, to r:uerilla morphologies under low resource supply. The clones establish ramets at high density (they torage intensively) given plentiful resources, and at low density (they 1arage extensively t when resources ;.re scarce. Thus, foraging activities <.re concentrated in sites from j,Jhich the rewards to the clone in lerms of resource acquisition will be greatest. Bells has described the ::tructure of clonal species like G. itederacea as consisting of feeding sites (rametsf separated by spacers tin C. hederacea these are stolons, :;lthough in other species they might be rhizomes, runners etc.). It is the spacers that provide much c-If the plasticity enabling either proliferation of feeding sites in r-source-rich patches of habitat, or movement away from resourcetleficient patches. (In some clonal species, however, selective placer-lent of ramets in favourable sites Eas been demonstrated without plasticity being shown to be the causey,ll.l

original parent

Fig. I. Experimental plants of Clechoma hederacea, la) a young plant, fb) an older plant

It is rarely possible to distinguish between the effects on clone morphology of resource scarcity caused by abiotic conditions and by competition. This, together with the other problems in studying plant foraging under held conditions which were outlined earlier, makes it difficult to interpret data from field studies as supporting the experimental results just described. Nevertheless, there are some data which appear to show similar forag-

showing the disposition

of ramets and stolons

in

ing responses in clonal species growing in the held, and some other data from controlled experiments. For example, white clover is more branched when grown in isolation than when grown in competition with grasses, when it displays greater linear extensionr2,1+. When grown experimentally under a leaf canopy, its stolon internodes are longer and branching is almost completely suppressed I4 comwith unshaded pared clones. 201

TREE vol. 3, no. 8, August

7988

(b)

80-

Rimary

stolons

Total stobns

(2 s E ) lengths of stolons and lb1 mean I 5 s EI number sets of experimental conditions. Dark bars: low light high nutrients. Modified from Ret 7.

Fig. 2. la) Mean

Clones of creeping buttercup from woodland (low light and probably competition for limited resources) had significantly longer internodes and a greater proportion of dry matter allocated to stolons than clones from adjacent grassland’5mt6. As in G. hederacea, experimental clones of creeping buttercup produce the same total length of primary stolon under high and low nutrient levels; there is a lower investment of dry weight per unit length of stolon, and far less under low nutrient branching, conditionsL7. Differential foraging in root systems and tree canopies It is not only in clonal herbs that differential foraging behaviour can be observed. Establishment of feeding sites should be greater in richer locations whenever resources are patchily distributed within the area of habitat being exploited by a plant. With this in mind, some earlier published results can now be interpreted in terms of foraging. Drew, Saker and Ashley’” reported experiments in 202

Primary ramets of ramets produced Hatched bars: high

Secondary ramets

Total ramets

per clone of Glechoma hederacw bhen grown under three light, low nutrients Light bars. high light, high nutrient<,

which different concentrations of nitrate were supplied to different zones of the primary roots of barley plants (see also Refs 19 and 201. Nitrate concentration exerted a strong localized effect upon accumulation of dry matter, and density and rate of growth of lateral roots, all of which were significantly greater in the zones of high nitrate concentration. As with primary stoIon production in clonal species, there was little effect of the concentration of supplied nitrate on either the extension rate or the final length of seminal root axes. Drew*O obtained comparable results in similar experiments using phosphate and ammonium. The casual observation that plant roots grow preferentially in areas of soil with favourable concentrations of inorganic nutrients4,2’-24 also supports the view that morphological plasticity promotes placement of feeding sites in areas from which resource acquisition should be most efficient. The structural complexity of tree canopies makes analysis of their foraging behaviour far more dif-

ficult, although Harper”,“’ distinguishes between guerilla species (e.g. Acer pseudoplatanus, Quercus robur, Fagus sylvatica, Eucalyptus spp.), which can extend long internodes at the ends of branches into light gaps, and phalanx species, such as members of the genera Picea, Abies and Cupressus, which are unable to do this because of tightly canalized growth forms. In cases where the canopies of adjacent trees meet, they may totally suppress each other’s efforts to forage for resources in the same three-dimensional space, with the result, as shown in Harper’%, that the two canopies confront, but do not interpenetrate each other, giving the visual impression of a single canopy. What happens to morphology when tree canopies, clones and root systems encounter parts of other plants attempting to occupy the same space and utilize the same resources is a subject that requires far more detailed study. Foraging in unproductive habitats Until now, differential foraging has been illustrated with examples

T‘7EE vol. 3, no. 8, August

1988

0. morphological plasticity. Howe{er, Crick and Grime26 may have identified a different foraging rctbsponse in species which charactfi~ristically grow in chronically unproductive habitats. Although resource supply is normally low under such conditions, mineral nutrients, for example, may become available at unpredictable times, in unpredictable patches, as a result of random decomposition or mineralization processes in the soil. Species of productive but highly exploited sites, such as many of those discussed in previous sections of this paper, are capable of rapid flux in root placement patterns, allowing roots to be projected into nutrient-rich Crick sites. and G-ime26 describe this as ‘active foraging’. in such species the turnover rate of the root system is high and the root : shoot ratio low. By contrast, species of unproductive habitats will have large root systems with a relatively static sp’atial distribution, a low turnover rate and a high root : shoot ratio. Ftinctional roots will be spread over a wide area, enabling exploitat on of pulses of nutrients without the need for great morphological plasticity. In unproductive sites a brief pulse of nutrients will probably have been absorbed by a plant with the latter type of foraging behaviour before the root system of an active forager can react to the pi:lse. As in most situations in plant ecology, it will be the occupant of a patch of ground which emerges as th.2 victor in competition for resources, rather than the prospectibe usurper. Responsiveness of differential foraging To produce efficient foraging in a heterogeneous environment, morphological plasticity must enable parts of the same plant encountering different conditions to grow in different ways. Responses to changes in the quality of the habitat must also be rapid. There is evidence from Glechoma hederacea that both of these requirements are met2,27. Evidence for the first came from experiments in which two halves of experimental clcsnes, connected by a single parent ramet, were provided with different resource levels to see ( I ) whether they would develop differen t morphologies, each of which

would correspond with that of clones foraging under the whole corresponding level of resource supply, or (2) whether physiological integration between the two halves would result in the development of an intermediate, compromise morphology throughout the whole of the clones. The results showed that each half of the experimental clones behaved as an independent substructure of the clone and that there was little if any evidence of integration via the connecting parent ramet2. The half of the clones receiving plentiful resources showed phalanx characteristics while the half receiving a low supply of resources developed guerilla characteristics. There was no evidence that the two parts of the clones adopted intermediate morphologies; few of their characteristics differed significantly from those of whole clones provided with the corresponding nutrient supply. This independent foraging behaviour in parts of the same clone will benefit the whole clone by promoting exploration of the most rewarding parts of the habitat rather than equal exploration of good and bad parts. Evidence of rapid morphological responses to changes in growing

11

-

conditions comes from experiments in which, as clones expanded, they were allowed to grow from resource-rich patches to resource-poor patches, or vice versa. Clones starting growth under resource-rich and resource-poor conditions displayed phalanx and guerilla morphologies respectively, as expected. However, the parts of the clones produced after growth into the opposite type of environmental patch rapidly assumed the appropriate type of morphology. Those clones growing from good to poor conditions ceased to display phalanx morphology; their parts produced under poor conditions rapidly adopted guerilla characteristics. Clones growing from poor to good conditions showed the reverse change (Fig. 3). The transitions were made quickly, indicating that plasticity is responsive enough to track small-scale environmental heterogeneity effectively to produce an efficient foraging behaviour27. Explaining differential foraging behaviour in plants As yet, little is known about the physiology underlying the changes in foraging behaviour as growing conditions alter. However, we can begin to speculate about mechan-

r

‘O-

5

z%I g5 0

1‘,

E ._

8-

7-

6

z iii

6-

? ‘z= 5CL 4

L1 1

I 2

I 3

I L

I 5

I 6

I 7

I 8

I 9

I 10

I II

1 12

Ramet number along stolon Fig. 3. Mean (2 s E1length of sequentially produced primary stolon internodes of experimental clones of Glechoma hederacea. In the treatment marked m-A the clones grew from high light, high nutrient conditions into low light. high nutrient conditions. In the treatment marked A--D the clones grew from low light, high nutrient conditions into high light, high nutrient conditions. From /kf 28.

203

TREE vol. 3, no. 8, August

isms in those species in which the spacers are stems or (like stolons and rhizomes) modifications of stems. For example, when a leaf canopy shades a plant, reducing incident light, it also transmits a higher far-red : red light ratio and a lower proportion of blue light than is found in unfiltered light2K.29 and this, rather than the reduction in photosynthetically active radiation flux, probably causes the morphological changes seen, by altering apical dominance and internode lengths7. There is some evidence for this in experimental work on stoloniferous white clover“l and tillering grasses30-jL. In addition, when soil nutrients, parin ticularly nitrogen, are limited supply, there is evidence of reduction in the synthesis of certain growth regulators, particularly cytokininjg,s4. Again, changes in cytokinin levels alter apical dominance internode lengths. and However, the control of morphology as growing conditions change is complex and requires further study. Conclusion Although plant ecologists have studied morphological plasticity for decades, they have tended to regard it more as a fate imposed upon plants growing under suboptimal conditions than a beneficial property. This view is rapidly changing. Plasticity to some degree compensates plants for being unable in most cases to move, and supplements the role of genetic

st~~t$

-

variation in promoting persistence range of growing in a wide condition9.h. It also confers the capacity for differential foraging for resources as growing conditions change. Although morphological plasticity may not be the only solution to the foraging problems of plants, the rapid progress which has recently been made in interpreting form in foraging terms suggests that this is a subject which will not only repay further attention, but strengthen the links between the research interests of plant and animal ecologists and plant physiologists. Acknowledgements I am grateful to Steve Waite tar valuable comments on an earlier version of this paper.

References

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2 Slade, A.1 and Hutchings. M J. 119871 1. Ecol. 75,95-l I2 3 Grime, I.P. II9791 Plantstrategiesand Vegetation Processes, Wiley 4 Grime, I P.,Crick, J-C. and Rincon. I E. S t B Symp. 40 I in press I 5 Slade, A.1. and Hutchings, M 1 I I9871 I Ecoi 75.639-650 I i, 6 Bradshaw. A.D II9651 Adv Cenet 115-155 7 Hutchings. M.I. and Slade, A j in Population Ecology of P/ants I Davy. A I Hutchings, M I. and Watkinson, A R edsi. Blackwell Iin press1 8 Bell, A.D II9841 in Perspectives on P/ant Population Biology (Dirzo. R. and Sarukhtin. I., edsl. pp 48-65. Sinauer 9 Eriksson. 0 I 19861 Oikos, ‘16, XL-X? IO Callaghan, T.V Headley. A.D., Svensson. B.M., Lixian, L., Lee, I A. and Lindlev. D K

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j IY861 Proc. R. Sac London Ser I3 228, I9 5-206 I I Salzman, A.C. I I9851 Soence 228,603-604 12 Harper, j_L 11983) in Evolution from Molecules to Men (Bendall, D S , ed 1, pp 32%345. Cambridge University Press I3 Harper, 1.L II9851 in Population Biology and Evolution of Clonal Organisms Ilackson. l.B C., Buss, L.W and Cook, R.E, edsl, pp l-3 3, Yale University Press I4 Solangaarachchi, S.M. and Harper, 1L II9871 Oecologia 72,372-376 I5 Lovett Doust, L t l98Il I Ed 69, 74-755 lb Lovett Doust, L. I I981 I / Eco/.69, 757-76X I7 Ginzo, H.D. and Lovell, P.H 11973) Ann Rot. 37,753-764 I8 Drew, M.C., Saker, L R and Ashley, 1 1ti 1197111. Exp Bot. 24, 1189-1202 I9 Wiersum. LK II9581 Acta Bot. Neerl 7 174-190 20 Drew, M.C I I975 I NewPhytol 75, 479-490 ol 21 Weaver, I.E I I9261 Root Development FieldCrops, McGraw-Hill 22 Weaver, I.E. and Clements, F t. I IY 381 P/antEco/ogyI:!ndednI,McCraw-Hill 23 Russell, E.W I I96 I I Soil Conditions and P/ant Growth 19th edn I, Longmans 24 Passioura, 1-B and Wetselaar. R I I Y72 I P/ant Soil 36, 461-473 25 Harper, I.L in Population Ecology ot P/ants (Davy. A I Hutchings, M I and Watkinson, A R edsl, Blackwell (in pressi 26 Crick, 1.C and Grime, I P (I9871 .NeLc f’hytol. 107, 403-Z I-1 27 Slade, A.\. and Hutchlngs, M 1 / I9871 / &CO/. 75, l023-IO36 28 Hutchings. M 1 1I9701 Ann Hot ,111 1207-I216 29 Holmes. M.C; f I% I I I” P/ants and the DaylightSpectrum (Smith. H ed I, pp I47- 158. Academic Press 30 Deregibus. V A., Sanchez, R.A. and Casal, I I I I983 I P/ant Physiol 72,900-902 31 Casal, I.I., Deregibus, V A and Sanchez. R.A t 1985) Ann Bat. 56 551-559 32 Deregibus. V A., Sanchez, R.A., Casal, I I and Trlica, M.I. I lYX51 1. ,App/ Ecol. 22. 109-206 33 Qureshi, F A. and McIntyre, G I I 1~7% can I Bat 57, IZZY-I235 34 Menzel. C M I I9801 Ann Bot 46. 25% 26’)

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