- Why we should conserve limiting factors, at least sometimes! - 573FORUMJournal of Vegetation Science 15: 573-575, 2004© IAVS; Opulus Press Uppsala.

AbstractKörner’s recent paper provided an excellent initial discussionof the term ‘limitation’ in ecology. I accept most of hisarguments but would argue that there are some circumstancesin applied ecology where the concept of limitation can beuseful; these are (1) where there is a deficiency of a factor thatprevents growth, and (2) where there is a need to manage anecosystem so that a limitation is enforced.

Keywords: Conservation; Management; Primary succession;Restoration ecology; Semi-natural community.

Körner’s recent paper

Limitation and stress – always or never provided anexcellent insight into two terms commonly confusedin ecology (Körner 2003). I agree with almost every-thing contained in this paper, but would argue that hedid not go far enough in his exploration of the term‘limitation’, or indeed what is a limiting factor acrossthe wide spectrum of potential usage in vegetationscience. To prolong this debate may seem pedanticbut there are situations in applied and restorationecology where the concept of limiting factors (usu-ally water or nutrients) can be used to describe accu-rately how ecosystems are functioning. As such it is auseful descriptor, especially for getting messagesacross to non-specialists, and I would not want to seeit scrapped unnecessarily.

Körner rightly points out that “Many people usethe term limitation whilst implicitly assuming limita-tion of certain metabolic processes or growth”. Indeedthe concept of the ‘law of limiting factors’ was origi-nally derived from constraints to population growth(Malthus 1798) or from scientists who were attemptingto increase agricultural production (Liebig 1856). In thelatter context, the limiting factors were derived fromadditive experiments, where addition of a ‘so calledlimiting factor’ increased production, or growth, be-cause a process-limiting constraint had been removed.

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Why we should conserve ‘limiting factors’, at least sometimes!

Marrs, R.H.

Applied Vegetation Dynamics Laboratory, School of Biological Science, University of Liverpool, PO Box 147,Liverpool L69 3GS, UK; E-mail calluna@liv.ac.uk

I would argue that perhaps a useful insight may behad by looking at the problem the other way round.Plant physiologists are comfortable with the concept ofessentiality, i.e. for water and essential nutrients there isa supply threshold that is needed to maintain basicphysiological function, below which the plant becomesdeficient and dies (Marschner 1995). Surely this is thepoint at which that factor becomes limiting. In restora-tion ecology this situation can either be a commonoccurrence, or a desire, and hence I would argue that theterm ‘Limiting factors’ retains a useful role in this areaof applied ecology.

Example 1: where factors genuinely limit

In the restoration literature (and literature on theearly stages of primary succession) there is good evi-dence for some situations where elements are truly limit-ing, i.e. the ecosystems do not function properly with thelevels of supply of these factors. For example, studies onthe restoration of kaolin wastes in Cornwall identified achronic lack of nitrogen during primary successions(Marrs et al. 1983; Marrs & Bradshaw 1993), at levelsthat did not allow the established plant species to growproperly and complete their life cycles. One example ofthis is shown in Fig. 1a, in this study the grasslandecosystem created during restoration became moribund;the grass was still living but only just. Only wherenitrogen was applied was there any increased growth.This is evident from the figure. However, what is notapparent from this figure was that where nitrogen wasnot added the vegetation did not just have a lowerproduction, it was showing real symptoms of nitrogendeficiency, i.e. the ecosystem was not working properlyas a result of a limiting factor: nitrogen. Thus, duringrestoration on such substrates, a nitrogen cycle needs tobe developed: this is done by accumulating sufficientsoil organic nitrogen, so that mineralization and othercycling processes can combine to supply a sufficient

574 Marrs, R.H. FORUM

Fig. 1. Evidence of nitrogen limitation in man-made primarysuccessions. a. Regrowth of moribund grass swards on kaolinwastes following N:P:K fertiliser application in factorial com-bination and in combination with an NPK addition (Rateswere 50 : 22 : 42 kg/ha of N:P:K; Bradshaw et al. 1975). b.Shoot extension of 10-yr old Acer pseudoplatanus on kaolinwastes between 1983 and 1986 in relation to proximity tonitrogen-fixing Alnus spp. (unpubl. data from A.J. Kendle &A.D. Bradshaw). Both diagrams augmented to illustrate nitro-gen deficiency\adequate supplies.

available-nitrogen supply for healthy plant growth(Marrs & Bradshaw 1993). This is borne out by obser-vations that when late-successional species such asQuercus spp. invade early in the restoration process, atbest they persist at the seedling stage until the nitrogensupply increases and then they can develop properly.More often the seedlings persist for some years, withminimal shoot growth and with leaves that are chlo-rotic, again showing symptoms of mineral deficiency.An example of poor tree growth is shown (Fig. 1b),

where Acer pseudoplatanus saplings show the benefit ofbeing planted near to nitrogen-fixing Alnus spp. Againwhat is not shown in the figure is the healthy growth ofthe trees which are growing actively, and the stuntedgrowth, where mineral-deficiency is present in the stuntedtrees, again a direct limitation by nitrogen.

In these situations, I would argue that nitrogen istruly limiting, in that the supply is so poor that it preventsthe proper functioning of individual species, and in somecases also of the ecosystem. The same phenomenon hasbeen found in old field successions (Bartha et al. 2003).

Example 2: where factors need to limit some species –a desire

In this case I agree with Körner that the term limita-tion is used, at best inconsistently, or at worst, incor-rectly. Studies on the conservation of semi-natural com-munities are littered with statements that the “communi-ties are limited by nitrogen and phosphorus” (Boeye etal. 1997; Lammerts et al. 1999; Güsewell et al. 2002;Turkington et al. 1998, inter alia). In my view this is thewrong use of the word, and whilst many of these publica-tions refer to limits to productivity (strictly correct use oflimitation if the Liebig view is correct) the implication isthat the ecosystems are nutrient-limited. This is notproven, because the communities exist, and can appar-ently function quite adequately, with the nutrient supplythat is already present at the site. The community haspresumably evolved under these conditions, and evi-dence for limitation is, as Körner complains, really theevidence of a response to nutrient addition. Essentially,in such studies what is measured is a pollutant effect.

In many cases. however, it is presumed that conserva-tion management should be implemented to either reducefertility, or maintain fertility at a low level (Marrs 1993).This requirement is especially important in the conserva-tion management of semi-natural biotopes such asheathlands and grasslands (Marrs 1993). This paradigmhad been derived empirically with relatively little realinformation about how infertile the conditions need tobe for community maintenance, i.e. how low does thenutrient supply need to be reduced so that some nutrientelements become limiting for some productive species.We have made empirical stabs at estimating target valuesfor soil available P in UK grasslands and heathlands;estimates vary from 15 - 20 mg-P.g–1 (Olsen-extract-able) (Gough & Marrs 1990; Critchley et al. 2002).These targets are essentially first approximations to alevel of limitation that allows many species to persist,but prevents other species with a high relative growthrate from growing productively, and hence out-compet-ing the slower-growing species.

- Why we should conserve limiting factors, at least sometimes! - 575FORUM

These estimates are crude, and there are three rea-sons for this. First, we rely for the most part on crudesurrogate measures of soil nutrient supply derived fromagriculture, viz. exchangeable or available concentra-tions, because we cannot measure rates of supply toplant roots accurately over long time periods. Second,we tend to over rely on additive experiments because itis easier experimentally to add nutrients to induce asurplus than it is to take them away to induce deficiencysymptoms. Finally, realistic measures of nutrient supplymust accommodate all aspects of the ecosystem, includ-ing competition with the below-ground components(Marrs 1993). This is difficult to measure, never mindcontrol, experimentally.

In conclusion

The aim of this paper was to augment the commentsmade by Körner on Limiting factors, to explain thatperhaps by clear definition we can still use the conceptto explain system behaviour in simple terms withinecology, and in conservation/restoration ecology in par-ticular. Does it matter? Like Körner, I believe thatdefinitions are important and there are two areas in theapplied conservation/restoration ecology literature wherea clear definition of the term Limitation is useful, indeedif expressed as above it may aid clear thinking andprovision of advice to practitioners.

Acknowledgements. I thank Ch. Körner for putting his headabove the parapet and thus allowing me to expose my preju-dices.

References

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Received 15 October 2003;Accepted 16 February 2004.

Co-ordinating Editor: S. Díaz.