Friday, February 27, 2015

The ‘size-advantage’ hypothesis for plant competition — rejected

  Plants with larger body size generally have lower fitness under severe competition.
The blue-flowered species has a larger maximum potential body size, but also must reach a larger size before it can reproduce at all — i.e. it has a larger minimum reproductive threshold size. In a severely crowded neighbourhood, therefore (represented here), very few offspring ever reach this minimum size and so they die without sex. In contrast, many offspring produced by the smaller red-flowered species — despite also being strongly suppressed by competition — manage to produce at least some grand-offspring, simply because they have a much smaller minimum reproductive threshold size.

Within most natural vegetation, resources are routinely and strongly contested between near neighbours of both the same and different species. According to conventional theory, the selection consequences of this sustained competition have been interpreted mostly in terms of a ‘size-advantage’ hypothesis — i.e. under severe neighbourhood crowding / competition, natural selection generally favours capacity (through pre-emptive, rapid and/or prolonged resource capture) for growth to a body size that is relatively large (e.g. Grime 1979; Keddy 1989, Grace 1990; Goldberg 1996). The precise physiological and morphological mechanisms of resource competition (particularly below-ground) may not always be size-related (Craine 2009). Nevertheless, since resources (water, soil nutrients, quanta of sunlight, etc) are always spatially (and temporally) distributed, it follows that a plant occupying more space (and over a longer time), both above and below ground, will generally be better equipped to acquire these resources and thus deny them to neighbours. An individual that manages to attain this relatively large body size (while neighbouring plants fail to do so) will thus, inevitably, be expected to achieve greater reproductive output. 

Results from recent empirical research, however, call into question the size-advantage hypothesis. If larger plant species are generally expected to exclude smaller ones when there is persistent crowding/competition, then neighbouring species should generally be more similar in body size than would be expected by random assembly, based on the local species pool. Yet several studies have failed to find evidence for this, including in grasslands (Schamp et al. 2011), old-field vegetation (Schamp, Chau & Aarssen 2008), wetlands (Weiher et al. 1998), temperate forests (Schamp & Aarssen 2009), tropical forests (Swenson & Enquist 2009), and coastal sand-dune succession (Waugh & Aarssen 2012). Larger species in crowded woody vegetation (Keating & Aarssen 2009), as well as in crowded herbaceous vegetation (Schamp et al. 2013, Aarssen et al. 2014), are not more likely than smaller species, to limit the resident species density within their immediate neighbourhoods, nor are they more likely to limit the representation of relatively small resident species. Bonser and Ladd (2011) similarly found that vegetative size was not a strong predictor of success under competition in annuals species; more important was the capacity to reproduce efficiently in the presence of competitors. Finally, a recent survey of published literature (Bonser 2013)—including for both short-lived semelparous and potentially longer-lived iteroparous species—showed that the efficiency of conversion of resources from vegetative tissue to reproductive output is generally higher (not lower) when competition levels increase, contrary to traditional life history theory.

When neighbourhood resources are strongly and persistently contested, therefore, there is apparently no general advantage (in terms of recruitment success or relative abundance within the habitat) for the offspring of species that are capable of (i.e. because they have evolved) relatively large potential body size (relative to the offspring of neighbouring species that have not evolved a large potential body size) (Tracey and Aarssen 2011, 2014). The vast majority of plant species everywhere are in fact relatively small; i.e. plant species body size distributions are right-skewed within every phylogenetic lineage, and for resident species at every spatial scale — from regional floras down to local neighbourhoods (Aarssen & Schamp 2002, Niklas et al. 2003, Aarssen et al. 2006, Poorter et al. 2008, Moles et al. 2009, Schamp & Aarssen 2009, McGlone et al. 2010, Dombroskie & Aarssen 2010, Tracey & Aarssen 2011). And importantly this is also true even within habitat types traditionally characterized as having the strongest competition effects imposed on resident species.

There is sufficient evidence, therefore, to reject the size-advantage hypothesis, and hence a need to replace it with revised model predictions for body size evolution in plants. The latter, I suggest, should begin with a now largely validated generalization: there is a fundamental between-species trade-off between maximum potential body size (MAX) and the capacity to reproduce when forced to remain small, i.e. minimum reproductive threshold size (MIN). This has long been evident anecdotally for woody vegetation (and see Thomas 1996, Davies & Ashton 1999), but has only recently been reported from empirical studies in herbaceous vegetation, including for the resident species within a single community (Tracey & Aarssen 2011, 2014, Nishizawa & Aarssen 2014). This ‘cost’ of relatively large body size likely reflects the need for generally greater investment in structural support tissue, and also structural or chemical defense against consumers — thus enabling the longevity (survival/growth time) needed in order to reach a large body size (Taylor et al 1990). This has implications for the interpretation of body size variation not just between habitat types — but also within a single community of interacting species.

Herein then lies a profound and largely overlooked implication for plant competition theory: if a larger species generally also needs to grow to a larger threshold size before it can reproduce at all, the latter may not be generally attainable in neighbourhoods with severe and persistent crowding / competition. Larger species, therefore, can certainly be successful competitors in terms of denying contested resources to neighbours, but not if they are unable to get large. And there can be no fitness (gene transmission) advantage at all in having a large body size unless the plant can reach, at least, its relatively large MIN. Accordingly, as argued below, it turns out that larger resident species within a plant community are not usually superior competitors when it really matters — in the most severely crowded neighbourhoods.

The 'reproductive economy advantage' hypothesis for plant competition.   

In the illustration above, hypothetical plants (genotypes or species) A, B, and C are represented by differently colored circles (white/gray/black) within three square ‘plots’ showing different neighborhood densities of resident seeds, which is the only stage in which the three plants – as embryos – are all the same size. In each case, the ‘stickplant’ symbols represent the relative body sizes of A, B, and C following emergence and growth to final developmental stage. The maximum potential body sizes (MAX) for A, B, and C can be expressed only when neighborhood density is very low (top row), where A has the largest MAX and hence the highest fecundity (represented by small red circles), and where it is thus favored by natural selection. Plant A therefore also has (as a trade-off) the largest minimum reproductive threshold size (MIN), which is expressed within a higher (intermediate)-density neighborhood (middle row). Here, plant B is favored by natural selection because its smaller MIN permits a higher fecundity than A, and its larger MAX permits a higher fecundity than C. Under very high neighbor density (bottom row), however, where all resident plants are severely suppressed in size, plant C has the highest fecundity because it has the smallest MIN (which imposes, as a trade-off, the smallest MAX) (Tracey and Aarssen 2014). Under these conditions, plants of both A and B die without sex because MIN for both is too large. Selection thus favours plant C because it has greater ‘reproductive economy’ — i.e. capacity to produce offspring that can survive long enough to produce at least some grand-offspring, while nevertheless remaining with a severely suppressed body size, even until death (Aarssen 2008).

Contrary to the ‘size-advantage’ hypothesis, therefore, selection in favor of relatively large MAX (plant A) occurs, not under the most crowded conditions, but only within local neighborhoods where competition effects are relatively weak (top row) — because only here can MAX (and its potential fitness advantage) be realized. The preponderance of relatively small resident species within most natural vegetation, therefore, can be at least partially accounted for by a preponderance there of severely crowded neighborhoods (bottom row).

Importantly here, success under severe competition is defined not just (or even most importantly) by capacity to capture resources and deny them to neighbours, but more fundamentally by the capacity to transmit genes to future generations, despite severe resource deprivation by neighbours. For this latter capacity, a growing body of evidence is pointing to an alternative hypothesis based on ‘reproductive economy advantage’: under conditions of extreme and protracted neighbourhood crowding/competition (where virtually all resident plants are necessarily forced to remain, until death, at only a small fraction of their maximum potential body sizes), it is the relatively small species that are more likely to leave descendants here — simply because they need to reach only a relatively small body size in order to produce at least some offspring. Resident plants of most larger species, however, are more likely to die here producing none at all.


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