Download Exceptions prove the rules

Exceptions
The most common form of exception to the simple predictions
of the various approaches to finding life histories that produce
an advantage to iteroparity is a variety of long-lived
semelparous species:
a variety of bamboo species
Agave, the century plant
The text appropriately points out that you need to distinguish
really semelparous species from those that reproduce
vegetatively, where each ramet is semelparous, but the genet
spreads reproduction out across ramets, so that the species is
‘almost’ iteroparous.
The two examples are really semelparous. The bamboo does
reproduce vegetatively, but all the ramets in the genet flower
simultaneously (in the same year). You’ll see the arguments
both documenting the semelparity and explaining why.
The reason the agave is a perennial semelparous (or
monocarpic) species is completely different, but the resulting
life history is similar.
The Bamboos
Many bamboo species are iteroparous perennials; these
grasses have more or less extended pre-reproductive periods,
then flower and set seed annually until senescence.
There are, however, a number of perennial, monocarpic
bamboos, and included among them seem to be all of the
economically important bamboo species.
Populations of these bamboos are, therefore, managed, and
natural cohorts are inevitably mixed with agriculturally
selected strains. Long-term genetic implications of the
apparent strategy may not, as a result, be easily testable.
Therefore, much of the study of semelparous bamboos has had
to be historical, rather than experimental.
Phyllostachys nigra
Phyllostachys bambusoides
Historical records indicate that a major Chinese bamboo
species, Phyllostachys bambusoides, flowered en masse (that
is simultaneously over hundreds of square miles) in 919 and
again in 1114, but not at any point in between. Cuttings of the
rhizomes of this species were brought to Japan and established
there. Those cuttings flowered during the period between 1716
and 1735, then again in 1844-1847, but not during any
intervening year (what happened between 1114 and 1716 is
not known).
Transplants from Japan, as well as the parental stock, flowered
next in the 1950's. Those transplants were scattered in
England, Russia, and Alabama among other places. All
flowered within 3-4 years of each other.
Flowering appears to be genetically programmed and fixed,
essentially unaffected by the enormous variation in
environmental conditions represented at its flowering sites
(Japan, England, European Russia, Alabama, etc.).
Many other bamboo species also flower in relative synchrony,
and with long intermast intervals. Many are exotic iteroparous
life histories. A partial list:
The range of intermast intervals in bamboos which flower
synchronously over large areas
.
Genera
Locations
Intermast Interval
Arundinaria spp.
Kenya, Himalayas
11 - >50
Bambusa spp.
India, Burma,Brazil
31 - 150+
Chusquea spp.
Jamaica, Chile,Brazil 15 - 34
Dendrocalamus spp. India, Burma
15 - 117
Phyllostachys spp.
China, Japan
13 - 120
The flowering in species like P. bambusoides is 'unique' in 2
ways. One is its freedom from environmental perturbation.
Unlike most other mast reproducing species like oaks,
beeches, and many fruit tree species (all of which have far
shorter inter-mast periods) there is no apparent environmental
cue to initiate mast year reproduction; unlike the others few
(almost certainly none) of the potential seed predators are
likely to survive the inter-mast period.
Yet seed predation is hypothesized by Janzen to be the
selective force behind this, as well as other masting
phenomena. Why?
Janzen’s basic reasons:
1) the seed crop can be extraordinarily large, and
2) the response and variety of seed predators can be
similarly extraordinarily large.
Why so many different seed predators?
Bamboo seed is slightly more nutritious than either rice or
wheat among commonly consumed grains in the human diet.
Among the 'natural‘ consumers are small rodents, wild pigs,
and jungle fowl (the progenitor of the domestic chicken).
The response of natural seed predators to this mast crop is
dramatic. The functional response includes an increase of 50100% in the number of eggs/clutch in the jungle fowl (an
indeterminate egg layer, but has a fixed brood size of 2).
Numerical responses through migrations are anecdotally
reported in the historical literature. Rat 'plagues' follow mast
years as a result of migration plus reproduction; in Africa
movements of flocks of weaver finches numbering in the
millions follow geographic 'migration' of the mast crops.
How large is the seed crop?
Seed crops 5-6 inches deep (a solid layer of seeds) below
parental stalks are observed. Larger seeded species prevented
accurate surveys by endangering the workers; seeds fell in
such profusion that equipment was damaged and workers
injured.
A crop of this size can satiate seed predators and permit some
of the seeds to escape predation to establish the next
generation.
But why is the masting cycle
1) so long and
2) so tight in timing?
There will be relative synchrony in flowering in bamboos
because they are wind-pollinated and apparently obligate
outcrossers. That alone would impose local synchrony; it
would cause high levels of local pollen flow, but severely limit
genetic exchange between demes.
Seed predators sharpen that synchrony, and impose it over
larger geographical areas.
How do seed predators affect synchrony?
Plants which anticipate the mast year (say by one year) are
unlikely to produce sufficient seed to satiate seed predators.
However, predator populations are likely to be of moderate
size, since there has been no recent mast crop, so it's possible
that a few seeds might escape.
Those that delay until after the mast year will face
insurmountable problems. They face predation from a fully
expanded predator population (from both functional and
numerical responses), and are very unlikely to escape seed
predation.
The loss of (selection against) genotypes which flower
slightly out of synchrony explains why the masting cycle is so
tight.
Only man, by lazily harvesting only when its easy, i.e. during
the mast year, but not years of limited seed crops, may select
against synchrony.
Mast year crops don't, in nature, wait around for slow-witted
predators. They germinate quite rapidly, and seedlings are not
heavily predated.
Why long inter-mast periods? How does an interval of
approximately 120 years evolve?
Janzen hypothesizes a scenario that begins with an annually
iteroparous bamboo (the most common life history among
bamboo species).
Seed predators are common, and escape of seed rare
(unpredictable reproductive success). An individual that
switched to semelparity (a chance mutation) should produce a
larger seed crop due to increased energy allocation to
reproduction. That crop might satiate the local, numerically
adapted population of seed predators and increase the
number of seeds escaping predation.
Now we have some annual semelparous individuals.
Their larger seed crop means that among escapees, offspring
of the semelparous mutant will slowly increase their
proportion in the population. The population becomes
dominated by, and eventually comprised entirely of annual
semelparous individuals (or semelparous, but with the same α
as the iteroparous kind) .
When the iteroparous parental stock has been completely
replaced, slight further shifts in  are strongly selected against.
This follows from the explanation for why timing is so tight.
Tails of the distribution of seed production are more
completely devoured than the peak, since seed predator
adaptations are designed for mast reproduction.
Janzen believed this switch would likely have been successful
only in the tropics. Predictable rainy seasons would bring
escape through germination, and the commonness of
territoriality among seed predator species in the tropics would
limit local numerical responses.
How are extremely long inter-mast intervals achieved?
Once semelparous, mutations that produce delay will be
selected for against the 'wild-type‘ (iteroparous) parental
stock. The longer these new mutants wait, the larger their
energy reserves, seed output, and success compared to
whatever increases in predation they draw to the seed crop of
the parental+mutant population. It isn’t clear that this delay
should occur as part of the initial switch to semelparity.
However, once entirely semelparous, delay that multiplies the
previous interval could prove selectively advantageous. Such a
mutation permits the bearer to produce larger numbers of
seeds than those who lack it, yet achieves the buffering
(protection) of producing seed simultaneous with the parental
populations.
The same kind of advantage that led to the switch to
semelparity now leads to replacement by a doubled-delay (or
tripled, quadrupled, …, but doubled is clearly the most likely)
population. Toward the end of the replacement process,
selection against the parental stock may be quite strong.
Here’s a commented diagram to indicate what (theoretically)
happens:
1) The initially iteroparous population, the height of the
vertical lines indicates the size of the seed crop.
2) Now a fraction of the population becomes semelparous. The
seed crop of those individuals is indicated by the second
line.
3) Now the population is entirely semelparous. Long delays
evolve by multiplication of the delay against a background
seed production of the older, shorter delay.
It's important to recognize there may be reasons other than
seed predator satiation that could explain extended delay.
Most 'tree-like' plants increase in biomass logistically. The
relative growth rate (the realized 'r‘) declines with size and
age; height growth and structural tissue are supported by a
'crown' of photosynthetic leaves that reaches a 'relatively'
constant biomass.
That's not true of bamboos. They are grasses reproducing
vegetatively to produce large genets in which each culm
(ramet) grows to full adult height, producing an adult
compliment of leaves and maintaining a green stem.
Photosynthetic and support tissues increase in parallel; genet
growth remains exponential over an extended period, and
biomass potentially available to allocation to reproduction also
continues to increase (exponentially) until mast seeding.
To indicate how common such species are Gadgil and Prasad
(1984) found that 70 of 72 Indian bamboo species were
perennial monocarps (long-lived and semelparous), but that
only 8 were synchronized over wide geographic areas.
The basic life history is, therefore, common, but Janzen's
arguments of the importance of mobile seed predators in
producing and synchronizing it possibly less common.
Let's consider seed production on the basis of flowering per
adult stem. Flowers on grasses are organized on spikes, with a
spike of flowers at each node (the slightly thicker rings on a
piece of dried bamboo).
Gadgil found in one of the synchronized, mast flowering
species, Bambusa arundinacea, the following flowering
rates:
65 flower bearing nodes/ramet
x 133 spikes per node
x 156 flowers per spike
= 1.3 x 106 flowers/culm at mast flowering
x 50-200 culms/genet
Even with the limitations of wind pollination, 24% of seeds
had developed endosperm, resulting in 150-800 Kg of
seeds/genet, and an allocation of biomass to reproduction of
between 20-30%. Not only is the total impressive, but the
allocation to reproduction in bamboos is far higher than in
trees (usually at most a few percent). This is without
reference to predators.
However, since the build-up to reproduction from clonal
growth may show variation due to environmental conditions,
the intermast interval and/or the intensity of reproduction may
vary over time. Since there may be variation among clones
and populations, we might also expect to see a broad peak in a
curve depicting intermast intervals. That is what Gadgil and
Prasad found…
What determines the optimum age for reproduction?
Aging! As new culms appear, older culms reach an age
when mortality rates increase. The optimum is set by the rate
of appearance versus age-related mortality. Genet
reproduction occurs before culm mortality increases,
‘wasting’ the biomass and energy committed to those culms.
The Agave story
Are seed predators the only external biotic force that drives the
evolution of long-lived semelparity? No!
That brings us to the other plant story – that of the century
plant, an Agave. First, the basis of the story:
In theory, any species should maximize the sum of current
fecundity (or mx) and expected future reproductive value
(which can be determined from proportional survivorship and
reproductive value of the next age class, i.e. px and Vx+1).
Graphing these two components on separate axes, a maximum
is achieved by greatest distance from the origin. Maximization
of the sum is, of course, the way to maximize fitness.
Remember the diagram…
If the curve is concave, maximum distance from the origin is
at one of the end points, i.e. either retain all energy for future
reproduction, or use all available energy.
Concave curves produce semelparity, with delay if, early on,
expectation of future reproduction exceeds possible present
offspring production.
For the bamboos the age of semelparous reproduction is set by
a mortality-driven decrease in residual reproductive value.
How does this apply to Agaves?
Residual
reproductive
value
Semelparous species
Heavy line indicates observed
strategy, here all energy reserved
As residual reproductive value until
Current benefit exceeds value of
retention for later reproduction.
In Agaves optimal foraging by pollinators will maximize the
seed set of individuals making the largest reproductive effort.
This, too, selects for semelparity in isolated, individual Agave
plants. If it costs a pollinator considerable energetic output to
get from one isolated plant to another, it should logically
choose those which offer the most food for the least flight
cost, i.e. those with more flowers (or greater reproductive
effort from the plant's point of view).
Evidence?
1. For the group of semelparous Agaves, but not for
congeneric iteroparous species, there is a significant
positive correlation between the percent of flowers which
successfully produce fruit and the size of the inflorescence.
Note that the positive correlation is with percentage of
flowers developing fruit. This corresponds to the
curvilinear profit function associated with semelparity.
Graphically:
2. The number of pollinators observed on a plant per
centimeter of inflorescence was positively correlated with
inflorescence length (which is proportional to the number of
flowers). More pollinators were attracted to each flower in
larger floral displays. This correlation was larger in
semelparous species of agave than in iteroparous ones, even
though the same pollinator, Bombus sonoris, works both
semelparous and iterparous agave species.
An interesting, but unanswered question, is why pollinator
selectivity should be different in agaves with differing life
histories when the flowers look virtually identical.