Bengtson 1 Introduction
“I before e, except after c, unless sounded as /ā/ as in neighbor and weigh”. We have all been
admonished to remember this rule. As ever in English spelling, though, there are exceptions with words
such as glacier, heist, and seize. In fact, there are more exceptions to this rule, 21 times more, than
there are adherents (QI 2010). This raises the issue of whether it might make more sense to amend the
rule. This is, in fact, what happened in the United Kingdom (Appendix 1). Likewise, in the 52 years
since the publication of Hardin’s (1960) competitive exclusion principle, far more examples of
coexistence have been found than adherents to the principle. Further, theoretical and empirical
advances have been made such that Hardin’s principle no longer reflects the current understanding of
the scientific community. It is worth contemplating, therefore, whether it is time to reconsider the
teaching of Hardin’s principle. That is, the ‘exceptions’ to the rule should be generalized and taught as
the rule, with the principle as an interesting, but perhaps unrealistic, case. In this essay, I review the
background of the principle and propose an alternate teaching perspective for undergraduates that
captures the broader context of coexistence and diversity in nature.
Background
According to Hardin (1960), “complete competitors cannot coexist”. This alliterative doctrine
forms the basis for the competitive exclusion principle. The economy and brevity of this phrase belie
much of the ecological theory at work behind the scenes. Hardin’s principle states that two distinct but
ecologically, behaviourally, and biologically identical species will not be able to occupy the same space
at the same time and use the same resources indefinitely; one species must eventually outcompete the
other. Additionally, the indefinite coexistence implies an equilibrium state in a system. This conclusion
was drawn from detailed laboratory experiments in Paramecium (Gause 1934) and Tribolium beetles
(Park 1954). As an aside, it is worth noting that the experimentally manipulated starting conditions,
such as temperature, humidity, and population density in Park’s experiments may have left some
Bengtson 2 competitors at a competitive disadvantage from the start. It is, therefore, interesting to note that the
excluding species was not always the same under all conditions. I will return to this aside later.
Hardly a year had passed before vociferous objections to Hardin’s ideas were published.
Hutchinson (1961) contested the assumption of equilibrium, stating that few, if any, systems ever reach
equilibrium. Otherwise stated, since exclusion is not an instantaneous process, a non-constant or nonhomogeneous environment increases the difficulty of achieving exclusion. From a practical
perspective, Hutchinson argues, the principle is of little value save as a starting assumption that can
then be quickly dismissed on the balance of evidence. This view has since formed the basis from which
coexistence has been investigated.
Such attacks and criticisms may, however, have missed Hardin’s point or, viewed more
favourably, been his intent. He wrote that “[f]or the present, [the] formulation [of the principle]…is
admittedly unclear; thus we can keep in the forefront of our minds the unfinished work before us.”
Hardin may thus have intended his article to be a rallying “call to arms” for empirical and theoretical
ecologists to go forth and investigate the limits of his principle and attempt to understand how and why
species coexist.
Having examined the principle’s historical context, it is necessary to jump forward some 30
years and discuss the issue of scale in biology. Levin (1992) sought to demonstrate the differences
among processes acting at local and regional scales. The scale at which coexistence and diversity are
measured plays a key role in their magnitude. α-, β-, and γ-diversity are measured at local scales,
among local scales, and at landscape scales, respectively (Whittaker 1960). Depending on the processes
at work, diversity at different scales can be simultaneously quite high or close to zero.
With these ideas and context in mind, I will broadly classify several example processes that
cooperate and contribute to promoting coexistence into two general categories, those that are fitness
equalizing and those that are fitness stabilizing, or frequency dependent, which together form an
Bengtson 3 alternate perspective from which to teach undergraduate students about coexistence in the natural
world.
Fitness Equalizing Processes
First, it is necessary to describe fitness before explaining its equalization among species. Fitness
is the ability of a species to survive and reproduce in an environment, relative to competitors. “Relative
to competitors” is crucial in distinguishing absolute fitness from relative fitness, a distinction between
an idealized competition-free environment and one that includes the fitness of competitors. A
competitor that is able to maintain a positive or neutral population growth rate, the equivalent of
relative fitness and the combination of reproduction and survival, while its competitors cannot, i.e. have
a negative growth rate, will be most fit among competing species and outcompete them in that system.
In such a system, it is not difficult to see that the greater the differences in relative fitness, the more
quickly competitive exclusion will occur.
Fitness equalizing processes act to reduce these differences. Such processes often involve trade
offs. In community ecology, a “Hutchinsonian demon” (Kneitel and Chase 2004) might dominate
because “it is the best at colonizing new patches, utilizing all the resources, avoiding predators and
resisting stresses”. In any environment where species face limited resources, the “demon” may be
forced to sacrifice ability to utilize one resource in order to utilize another. Trade offs may, therefore,
represent niche differentiation and explain some instances of coexistence (Chase and Leibold 2003).
Returning to the aside, one might speculate that Park’s beetle species might have coexisted at some
intermediate level of temperature or humidity where neither could gain the competitive upper hand.
Under warmer temperature, one species might have been favoured, while the other might have been
better suited to lower temperatures.
Another common trade-off occurs between dispersal and competitive ability, which has, for
several decades, been used to explain community patterns on a wider scale. MacArthur and Wilson
(1967) proposed in their theory of island biogeography that the number of species on an island was the
Bengtson 4 result of a balance between immigration and extinction. On islands where species face a high likelihood
of extinction, diversity will be low unless the immigration of a number of species is also high. More
recently, island biogeography has been applied to metapopulation theory, the body of research
concerned with populations linked by dispersal. The resultant metacommunity concept, regarding
communities of species linked by dispersal, is a current hotbed of research into coexistence. It states
that in a patchy environment, species trade off their ability to disperse and compete. A good disperser is
generally poor at competing with a species that competes well but disperses poorly. Thus where
dispersal is low, the competitor will drive the disperser to local extinction and diversity will be low.
Where dispersal is high, communities may become homogenized, with diversity again being low. Thus,
at some intermediate level of among-patch dispersal, the greatest number of species can coexist locally
(Mouquet and Loreau 2003).
The above ought to be tractable at the undergraduate level, but a brief search of ecology
textbooks indicates that dispersal is limited to topics of populations (e.g. Molles 2008) and does not
feature in the discussion of competition. Further, the explanatory ability of the metacommunity concept
has moved from the realm of theory to that of empirical research (e.g. Cadotte 2006a). The theory of
limiting similarity was first mentioned in 1967 and by 1978 was in several standard textbooks (Abrams
1983). The term metacommunity was first introduced some 20 years ago (Gilpin and Hanski 1991).
The metacommunity concept specifically and fitness equalizing mechanisms in general deserve to be
included in undergraduate ecology textbooks.
Frequency Dependent Processes
Processes that are frequency dependent act in such a way that the more or less prevalent a
species is in a system, the greater or less will be the force acting upon it. Under positive frequency
dependent processes, the more common a species becomes, the more fit it will be. If finding a mate is
difficult or time-consuming, for example, then a rare species may be less fit than a common one
because they must devote a greater amount of time or effort to finding a mate relative to producing
Bengtson 5 offspring (Greene and Stamps 2001). In between-species competition, it is not difficult to see how this
might lead to reduced diversity. Negative frequency dependence represents the opposite effect, in
which a rare species is more fit that a common one, specifically because it is uncommon. This is in fact
a hallmark of coexistence mechanisms generally; they must not show any long-term trends in species
abundances. In other words, if a species becomes rare, it will then have a positive growth rate (Chesson
1994, 2000). This is commonly referred to as the ‘rare species advantage’ and is a way to reduce the
intensity of competition faced by such species. The processes that fall under this heading are some of
the more classic criticisms of Hardin’s principle and are likely taught to a greater or lesser extent in
ecology courses, but still as exceptions to the rule.
Natural environments are not homogeneous. Heterogeneity in space allows species refuges from
competition in patches within low-dispersal systems (Appendix 2). Such low-dispersal systems are
characterized by decreased local diversity, but high among-patch and/or regional diversity. Because
dispersal is limited, the possibility of colonization by a superior competitor and subsequent
displacement of the regionally more-rare species is thus diminished. From the standpoint of Hardin’s
principle, it is tempting to declare the principle valid in such a system, since local diversity is low and
may even be nonexistent. Such a conclusion ignores processes and coexistence occurring at wider
scales.
Predation and parasitism are also examples of negative frequency dependence. From the
perspective of the predator or parasite, the most numerous target or host that will most easily benefit
the predator or parasite thus maximizing its fitness should be preferentially targeted. Predators form a
search image when hunting prey, which is composed of sensory inputs and is assumed to be heritable
(Pyke et al 1977). It follows then, that the more abundant of two competing species will more often
show up in that search image and so be more frequently preyed upon. This lowers the common species’
abundance, permitting the less frequent species to flourish in the absence of predation. Over time, the
rarer species might become the numerically dominant competitor. If the predator is able to switch
Bengtson 6 specializations among competing prey species within few generations, then predation can be
considered a coexistence mechanism (Abrams and Matsuda 2003). The same process has also been
demonstrated in Daphnia- (Ebert 2008) and snail- (Lively and Dybdahl 2000) parasite systems.
Paine’s (1966) work on trophic dynamics suggested that more stably productive environments
are able to support more predators who, specializing on different prey types, permit more diversity and
coexistence. This statement, if true, fundamentally undermines the validity of Hardin’s principle. I will
limit this to a thought experiment, one which could be undertaken in an undergraduate ecology course.
A mature forest would be more likely to have a constant level of production relative to a frequently
disturbed environment. The latter has the potential for low production or very variable production by
virtue of loss of productive biota and insufficient time for trophic relationships to develop via
immigration. If Paine’s statement holds, and a stably productive environment can be considered in
equilibrium, then it provides another reason not to teach Hardin’s principle as exclusively.
Species may respond in a variety of ways to temporal heterogeneity in their environments. In
particular, the storage effect (Chesson 2000) is a way of maintaining diversity among competitors who
compete in space, but not at the same time. Daphnia resting eggs and plant seed banks are examples of
the storage effect. Under the storage effect, species emerge and compete at a time when they are most
fit and can thus leave behind the greatest possible number of offspring. Several competing species
might thus emerge separately and alone, effectively treating their common environment as a timeshare. Species are then competing against themselves more than they are against other species, or when
intraspecific competition is stronger than interspecific competition. A rare species will be able to
emerge and compete at a time when numerically and competitively dominant species are dormant.
Temporal variability can also take the form of a disturbance or environmental perturbation.
Disturbance alone, however, does not represent a coexistence mechanism because it can
indiscriminately and proportionally affect all members of a community, rather than selectively
targeting the more common species (Chesson and Huntly 1997). The intermediate disturbance
Bengtson 7 hypothesis is dependent on where species fall on the competition-colonization trade off spectrum
(Cadotte 2007). It is therefore that trade-off, discussed above, which promotes coexistence.
Conclusion
Teaching the debate on coexistence from the perspective of the types of mechanisms that
promote coexistence rather than the small minority of mainly, perhaps, laboratory cases that
demonstrate exclusion, would bring teaching in line with current thinking (Chesson 2000, Adler et al
2007, Ostling 2011). Explaining Hardin’s principle may represent a useful starting point, but as a
principle was outmoded before it was published (e.g. Hutchinson 1941). Hardin intended his principle
to be a “call to arms”, which it has certainly been. If, however, an undergraduate completes a
biology/ecology degree knowing only that complete competitors cannot coexist, they leave having
learned that nothing in ecology has fundamentally changed in the past 50+ years, which is
demonstrably not the case. Instead, biology undergraduates should learn that the principle is a useful
starting point that can explain diversity patters in certain controlled situations but that coexistence of
species with similar competitive abilities can and, more often than not, do co-occur in nature as a result
of a balancing act between fitness equalizing processes such as trade offs and fitness stabilizing
processes like the rare species advantage.
Bengtson 8 References
Abrams, P. 1983. The theory of limiting similarity. Annual Review of Ecology and Systematics 14: 359376.
Abrams, PA and H Matsuda. 2003. Population dynamical consequences of reduced predator switching
at low total prey densities. Population Ecology 45: 175-185.
Adler PB, J HilleRisLambers, and JM Levine. 2007. A niche for neutrality. Ecology Letters 10: 95-104.
Cadotte, MW. 2006a. Metacommunity influences on community richness at multiple spatial scales: a
microcosm experiment. Ecology 87: 1008-1016.
Cadotte, MW. 2006b. Dispersal and species diversity: a meta-analysis. American Naturalist 167: 913924.
Cadotte, MW. 2007. Competition-colonization trade-offs and disturbance effects at multiple scales.
Ecology 88: 823-829.
Chase, JM and MA Leibold. 2003. Ecological niches: linking classical and contemporary approaches.
University of Chicago Press, Chicago, IL, USA.
Chesson, P. 1994. Multispecies competition in variable environments. Theoretical Population Biology
45: 227-276.
Chesson, P. 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and
Systematics 31: 343-366.
Chesson, P and N Huntly. 1997. The roles of harsh and fluctuating conditions in the dynamics of
ecological communities. American Naturalist 150: 519-553.
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Conventions.
http://webarchive.nationalarchives.gov.uk/20110809091832/http://teachingandlearningresources.
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Ebert, D. 2008. Host-parasite coevolution: insights from the Daphnia-parasite model system. Current
Opinion in Microbiology 11: 290-301.
Gause, GF. 1934. The struggle for existence. Williams and Wilkins, Baltimore, MD, USA.
Gilpin, M and I Hanski. 1991. Metapopulation dynamics: empirical and theoretical investigations.
Academic Press, London.
Greene, CM and JA Stamps. 2001. Habitat selection at low population densities. Ecology 82: 20912100.
Hardin, G. 1960. The competitive exclusion principle. Science 131: 1292-1297.
Hutchinson, GE. 1941. Ecological aspects of succession in natural populations. American Naturalist
75: 406-418.
Hutchinson, GE. 1961. The paradox of the plankton. American Naturalist 95: 137-145.
Kneitel, JM and JM Chase. 2004. Trade-offs in community ecology: linking spatial scales and species
coexistence. Ecology Letters 7: 69-80.
Levin, SA. 1992. The problem of pattern and scale in ecology. Ecology 73: 1943-1967.
Lively, CM and MF Dybdahl. 2000. Parasite adaptation to locally common host genotypes. Nature
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Bengtson 9 MacArthur, RH and EO Wilson. 1967. The theory of island biogeography. Princeton University Press,
Princeton, NJ, USA.
Molles, M. 2008. Ecology: concepts and applications. McGraw-Hill, New York, NY, USA.
Mouquet, N and M Loreau. 2003. Community patterns in source-sink metacommunities. American
Naturalist 162: 544-557.
Ostling A. 2011. Do fitness-equalizing tradeoffs lead to neutral communities? Theoretical Ecology
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Paine, RT. 1966. Food web complexity and species diversity. American Naturalist 100: 65-75.
Park, T. 1954. Experimental studies of interspecies competition II. temperature, humidity, and
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Bengtson 10 Appendix 1
The below is copied from the United Kingdom’s Department for Education Teaching and Learning
Resources’ section on Spelling Guidelines and Conventions for Primary students.
I before e except after c
The i before e except after c rule is not worth teaching. It applies only to words in which the ie or ei
stands for a clear /ee/ sound and unless this is known, words such as sufficient, veil and their look like
exceptions. There are so few words where the ei spelling for the /ee/ sound follows the letter c that it
is easier to learn the specific words: receive, conceive, deceive (plus the related words receipt,
conceit, deceit), perceive and ceiling.
Appendix 2
Figure taken from Cadotte (2006b) who adapted it from Mouquet and Loreau (2003). It shows a
hypothesized relationship between dispersal and species richness at three different spatial scales.