The opposing paradigms in resource limitation on plant growthpost.queensu.ca/~biol953/Casper Christiansen - The opposing paradi… · Plant growth is said to be limited when a resource

The opposing paradigms in resource limitation on plant

growth

By Casper Tai Christiansen

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Introduction

Resource limitation on growth is one of the oldest fundamental concepts in ecology. In the past century,

numerous studies have dealt with questions like how or when limitation occurs but despite these efforts

many unanswered questions remain. Plant growth is said to be limited when a resource is taken up at a

rate less than the plant’s demand for that resource. Growth is then limited by the supply of that

resource. For plants, necessary resources are carbon, nutrients and water – which they must obtain from

the atmosphere and soil. Although resource limitation may occur for all types of organisms, the focus

of this essay is restricted to the one of plants. The seminal paper The Ecology and economics of storage

in plants by Chapin, Schulze and Mooney (Chapin et al. 1990) owes much – if not all – of its micro-

economical frame work to earlier work by Arnold Bloom and colleagues (1985, 1986). Briefly, plants

should – much like business firms – seek to maximize growth (i.e. profit) through optimizing the

efficiency of resource acquisition and allocation. As a plant acquires resources – these are then

allocated to new biomass – and how these newly obtained resources are differentiated between plant

organs (i.e. leaves, stems and roots) strongly affect the continued uptake of resources. While storage

provides plants protection from fluctuating supplies of resources (Chapin et al. 1990) – and thus may

accommodate growth in times of poor resource availability – this essay will focus on two theories of

vegetative plant growth limitation by said resources.

Opposing paradigms in growth limitation

Our understanding of nutrient limitation on growth has for the majority of the 20th century been one of

single-nutrient limitation. This is the law of the minimum (LOTM) – co-originated by Sprengel (in

1828) and Liebig (in 1855) (see Craine 2009). Essentially it states that plant growth is limited by one –

and only one – single resource at any one time. It is only after the demand is met for that one resource

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that another resource may become limiting (see Appendix Figure A1). The emergent paradigm,

however, is the hypothesis of multiple resource limitation (MRL) (Chapin et al. 1987, Gleeson and

Tilman 1992). According to Bloom et al. (1985) “Plants should adjust allocation so that all resources

equally limit growth”. For example, if carbon is abundant and nitrogen is scarce, the plant should

allocate relatively more resources into root proliferation in order to improve nitrogen uptake, i.e.

change its root-shoot ratio. By doing so, plants actively create a dynamic balance where all resources

should be equally limiting to growth (Bloom et al. 1985). As we shall see later in this essay, the MRL

predicts that an increase in any one resource should increase plant growth. This contrasts with LOTM –

where only an increase in the supply of the limiting resource would have a positive effect on growth.

Argument

In the years following Bloom et al.’s (1985) work, the MRL hypothesis was incorporated into

ecological theory (Chapin et al. 1987, Gleeson and Tilman 1992) and became the new emerging

paradigm, replacing the law of the minimum. Above, I have briefly introduced the two hypotheses on

resource limitation on plant growth. In the following text, I will then review their assumptions and

predictions and relate this to a selected body of studies on resource limitation, and especially co-

limitation. In the last paragraph of their paper, Bloom et al. (Bloom et al. 1985) postulates: “This

theorem describes growth in relation to resource limitations more accurately than does Liebig’s law of

the minimum” – a bold statement. But how well do the two paradigms really fit with empirical

observations? In this essay, I will argue that while MRL has greatly improved our understanding of

plant growth both MRL and LOTM are necessary to adequately explain observations on resource

limitations in plant communities – and I will argue that this is because of the assumptions upon which

the theories are based as well as the nature of plant-nutrient requirements.

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The plant as an active forager

When exposed to low light, plants usually respond by increasing allocation of biomass to leaves.

Likewise, plants enhance root biomass when faced with low soil nutrient availability (Chapin 1980, and

references therein). These plastic responses in plants have been attributed to their active role in

acquiring resources (Grime 1979, Chapin 1980). Much like motile animals forage for food so do sessile

plants. Adaptive plant uptake assumes that plants are selected to optimize allocation of one resource

(think of it as a currency) in exchange of a different resource from the surroundings (Bloom et al.

1985). Basically, we are dealing with exchange ratios between resources (e.g. carbon for nitrogen – as

with currencies, Canadian dollars for Euros). Plants should avoid excess foraging for a non-limiting

resource and maximize effort into acquisition of a limiting resource. This is achieved through variation

in physiology and morphology – as imposed by plasticity, genotype and species differences. Simply

put, the optimal foraging strategy would be the one where plants take up resources in precisely the

proportion needed for growth. In theory, this would then lead to all resources effectively being limiting

and an increase in any resource should enhance growth (Bloom et al. 1985, Gleeson and Tilman 1992).

The law of the Minimum

Originally developed for individual plants in agriculture to enhance yield, the law of the minimum has

since been applied to a diverse field of wild plants and whole communities (Danger et al. 2008). LOTM

was formulated for nutrients only and contains three parts: a) Growth is limited by the resource that is

supplied the least relative to its demand, b) growth is proportional to the supply of the limiting resource,

and c) growth cannot increase by addition of a non-limiting resource (Craine 2009). Leibig assumed

that plants did not actively influence nutrient availability, but there are several ways of which plants

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may do so; e.g. root-shoot adjustment, mykorrhizal symbiosis, root exudation of labile carbon rich

substrate, and release of other compounds such as phosphatases (Craine 2009, and citations therein).

Plants are indeed actively foraging, and should therefore be balancing their resource uptake. However,

this does not necessarily mean that LOTM doesn’t still apply.

Testing of single resource limitations

A simple way to test a hypothesis stating that LOTM applies better to plant growth limitation than

MRL could be to supply plants with e.g. nitrogen (N) and phosphorous (P) in a factorial design and

then observe the response in growth. If plants supplied with N increase in biomass then it follows that

N was the limiting resource and that the same plants should not respond to P (See Appendix A-2).

However, if plants also respond to P with increased growth – then MRL would seem to apply.

Depending on what paradigm you support, the literature has plenty of supporting examples to take

from. For example, observations by Tilman (1987, 1990) indicate that single resource limitation

(primarily N) applies to plant growth. Likewise, Gleeson and Tilman (1992) discuss responses in plant

growth following single additions of both water and nutrients. Are both MRL and LOTM right? Are

they wrong? I would like to approach this by continuing into co-limitation of resources.

Co-limitation in MRL and LOTM

MRL predicts co-limitation by all resources (Bloom et al. 1985, Gleeson and Tilman 1992). Contrary to

what one might expect, LOTM may allow for two scenarios of co-limitation. These are simultaneous

co-limitation and serial limitation (see Appendix A-3). Simultaneous co-limitation is a special way of

viewing LOTM where supply relative to demand for two resources is equally limited. Thus, only when

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resources are added together growth occurs. However, as nutrient supply and demand greatly vary this

kind of limitation should not occur frequently in a LOTM world. Recent plant community meta-

analyses have shown substantial serial limitation of N and P (Elser et al. 2007, Harpole et al. 2011)

across both aquatic and terrestrial plant ecosystems. That is; a synergistic response to a second nutrient

only after addition of a ‘primary’ limiting nutrient. This fits nicely into the LOTM hypothesis.

However, (Harpole et al. 2011) showed that slightly more studies (28% vs. 22%) displayed strict co-

limitation compared to serial limitation, favoring MRL. But when adding together studies showing

single limitation and serial limitation the numbers were higher than studies showing strict co-limitation,

indicating that LOTM indeed has a role to fill regarding plants (Harpole et al. 2011). The question

remains, why do we see these apparently contrasting responses in plant growth?

Dealing with assumptions

MRL theory assumes that plants’ stoichiometric requirements are equal (Bloom et al. 1985). But plant

stoichiometric requirements are variable between species (Craine 2009) and recent evidence also shows

that they may change with age, or rather: plant size (McCarthy and Enquist 2007, and references

therein). If plant stoichiometric requirements are species dependent and age dependent then it seems

plausible that plant communities – i.e. an assemblage of different species and ages – should be limited

by a variety of resources. Danger et al. (2008) argues that communities, unlike single species, are likely

to adjust their stoichiometry to resource supply through competitive exclusion and co-existence

mechanisms. Plant communities may be composed of multiple species either sharing or inhabiting

distinct niches. If niches overlap then the community will be more likely to be limited by few or a

single resource (that all species are adapted towards), but if niches are unique then a greater variety in

limiting resources should arise. Due to competitive exclusion theory (Hardin 1960), co-existing species

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should vary to a certain extent and thus co-limitation of resources at the community level would be

expected. The problem of scale (Levin 1992) comes to mind here – scaling from single plant species to

communities – but also over time due to plant size imposed differences in stoichiometric requirements.

Another critical assumption in MRL theory is that resources can be substituted to a varying degree by a

common currency, e.g. carbon (Bloom et al. 1985). For example, if nitrogen is limiting plants may

substitute it with carbon, using phenolics instead of alkaloids in herbivore defense structures (Bloom et

al. 1985). But can everything be substituted for something else? Take RUBISCO (Ribulose-1,5-

bisphosphate carboxylase oxygenase) as an example which is the most abundant protein in the world

(Hopkins and Huner 2004) – vital for plant photosynthesis. It contains a magnesium complex which

cannot be substituted with a different resource. Without magnesium there is no RUBISCO and

therefore no photosynthesis, i.e. no plant growth.

Conclusions

This short review of the two opposing paradigms in plant resource limitation on growth has highlighted

some key issues associated with the way we perceive limitation. First, plants are active foragers seeking

to balance resource uptake. This fits perfectly with the MRL and economic theory. However, LOTM

still have validity as shown in the meta-analyses of N and P limitations on plant communities. But what

does a study on N and P addition really tell us? An ongoing experiment in Alaska has shown enhanced

plant biomass following long-term fertilization with N+P (Shaver et al. 2001). But the changes in

biomass were not uniform across species; dwarf birch (Betula nana) was the species with the greatest

growth response. Does this mean that the other species weren’t resource limited? No, probably not. But

what it does mean is that the birch species is better at adapting to increased N+P supplies, thereby out-

competing other species of plants. One could argue that it is an example of the Tragedy of the

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Commons (Hardin 1968); plant resources are available to a number of species but if one particular

species acquires more, then the rest will suffer from limitation. An important point to make is that

while we are talking resource limitations on plant growth, almost all examples shown have been on soil

nutrients. This is no coincidence. Most studies on plant resource limitation have indeed been performed

on soil nutrients. Experiments with increased water or light are rare and co-limitation studies on

potential light and nutrient co-limitation even more so. So what does N and P addition studies tell us?

This depends highly on the interpretation of results. For example, the single resource limitation

illustrated in Appendix A-2 b) may show N as the limiting factor on plant growth. But it could also be

that another resource is limiting – a resource not tested for. In the study from Alaska mentioned above,

potassium could potentially be more limiting for other species than birch, and thereby contribute to the

observed response in community composition. Nitrogen is a key nutrient in photosynthesis and N-

content in leaves is strongly correlated to photosynthesis (Hopkins and Huner 2004). Therefore it seems

intuitive that N more strongly regulates growth than other nutrients used to lesser extent. If some

nutrients are relatively more important to plant growth than others, and some may be substituted for

others while others may not be, then why should we assume that limitation of any one resource would

yield the same results? Or if nitrogen is limiting why should an increase in magnesium supply improve

growth? Rather, we should look at nutrients as being either limiting in different ways – and not

generalize and expect equal responses in plants to all resources. For example, nitrogen and phosphorous

additions may often induce synergistic growth responses in plants (i.e. MRL response), while when e.g.

magnesium is limiting, then only magnesium supply will lift the limitation on growth. Furthermore,

our understanding of resource limitation on growth would benefit greatly from expanding from the

usual suspects, i.e. N and P, to including other nutrients and especially light and water manipulations in

a factorial design. We should balance our view of limitation to include all resources – or at least a more

balanced contribution from the vast pool of potentially limiting resources.

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References

Bloom, A. J. 1986. Plant Economics. Trends in Ecology & Evolution 1:98-100.

Bloom, A. J., F. S. Chapin, and H. A. Mooney. 1985. Resource Limitation in Plants - an Economic

Analogy. Annual Review of Ecology and Systematics 16:363-392.

Chapin, F. S. 1980. The Mineral-Nutrition of Wild Plants. Annual Review of Ecology and Systematics

11:233-260.

Chapin, F. S., A. J. Bloom, C. B. Field, and R. H. Waring. 1987. Plant-Responses to Multiple

Environmental-Factors. Bioscience 37:49-57.

Chapin, F. S., E. D. Schulze, and H. A. Mooney. 1990. The Ecology and Economics of Storage in

Plants. Annual Review of Ecology and Systematics 21:423-447.

Craine, J. M. 2009. Resource strategies of wild plants. Princeton University Press, New Jersey.

Danger, M., T. Daufresne, F. Lucas, S. Pissard, and G. Lacroix. 2008. Does Liebig's law of the

minimum scale up from species to communities? Oikos 117:1741-1751.

Elser, J. J., M. E. S. Bracken, E. E. Cleland, D. S. Gruner, W. S. Harpole, H. Hillebrand, J. T. Ngai, E.

W. Seabloom, J. B. Shurin, and J. E. Smith. 2007. Global analysis of nitrogen and phosphorus

limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecology

Letters 10:1135-1142.

Gleeson, S. K. and D. Tilman. 1992. Plant Allocation and the Multiple Limitation Hypothesis.

American Naturalist 139:1322-1343.

Grime, J. P. 1979. Plant strategies and vegetation processes. John Wiley & Sons, New York.

Hardin, G. 1960. Competitive Exclusion Principle. Science 131:1292-1297.

Hardin, G. 1968. Tragedy of Commons. Science 162:1243-&.

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Harpole, W. S., J. T. Ngai, E. E. Cleland, E. W. Seabloom, E. T. Borer, M. E. S. Bracken, J. J. Elser, D.

S. Gruner, H. Hillebrand, J. B. Shurin, and J. E. Smith. 2011. Nutrient co-limitation of primary

producer communities. Ecology Letters 14:852-862.

Hopkins, W.G. and N. P. A. Huner. 2004. Introduction to Plant Physiology. 3rd Edition. John Wiley &

Sons, Hoboken.

Levin, S. A. 1992. The Problem of Pattern and Scale in Ecology. Ecology 73:1943-1967.

McCarthy, M. C. and B. J. Enquist. 2007. Consistency between an allometric approach and optimal

partitioning theory in global patterns of plant biomass allocation. Functional Ecology 21:713-

720.

Shaver, G. R., S. M. Bret-Harte, M. H. Jones, J. Johnstone, L. Gough, J. Laundre, and F. S. Chapin.

2001. Species composition interacts with fertilizer to control long-term change in tundra

productivity. Ecology 82:3163-3181.

Tilman, D. 1987. Secondary Succession and the Pattern of Plant Dominance Along Experimental

Nitrogen Gradients. Ecological Monographs 57:189-214.

Tilman, D. 1990. Constraints and Tradeoffs - toward a Predictive Theory of Competition and

Succession. Oikos 58:3-15.

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Appendix A-1

Figure A-1. The law of the minimum can be visualized by the barrel analogy. Each individual stave

represents a resource (e.g. nitrogen or water) and the height of the stave corresponds to the supply of

that resource relative to the plant’s demand. Plant biomass is equal to the level of water inside the barrel

– and growth is therefore strictly limited by the height of the shortest stave, i.e. the supply of the most

limiting resource. Increasing the supply of this resource increases the height of its corresponding stave

and the barrel will be able to hold more water. If the stave becomes longer than another stave then the

resource associated with that stave will change status to the most limiting resource, and plant growth

will not increase until the supply for that resource is enhanced.

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Appendix A-2

Plant growth responses to factorial additions of nitrogen (N), phosphorous (P), and combination (N+P)

thereof. Control is (C).

a) No response to nutrient additions.

b) Single resource limitation, when plants are limited by one resource only. In this example, N is

the limiting resource. Addition of P does not enhance plant biomass.

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Appendix A-3.

Possible co-limited responses to factorial additions of nitrogen (N), phosphorous (P), and combination

(N+P) thereof. Control is (C). This figure was redrawn and edited from Harpole et al. (2011).

a) Simultaneous co-limitation, when two (or more) resources limit growth simultaneously. In the

example above, growth does not increase until both N and P are added together. Growth is

dependent on both resources becoming available.

b) Independent co-limitation, when single resource additions increase growth. Both N and P limit

growth in this example, however, single additions of either resource enhances growth. Added

together, N+P may further enhance growth in a synergistically fashion (as shown).

c) Serial limitation, when the response to a second resource is determined by addition of a prior

resource. In the example above, single N addition does not increase biomass while P does.

However, when added together, there’s a synergistic effect of N+P and biomass increases the

most when the two resources are added together.