Exceptions

1. 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

2. 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.

3. 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.

4. Phyllostachys nigra Phyllostachys bambusoides

5. 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.

6. 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 . GeneraLocationsIntermast 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

7. 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.

8. 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 50-100% 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.

9. 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?

10. 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.

11. 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.

12. 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.

13. 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.

14. 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.

15. 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.

16. Here’s a commented diagram to indicate what (theoretically) happens: • 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.

17. 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.

18. 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).

19. 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.

20. 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…

23. 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.

24. 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…

25. 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?

26. Heavy line indicates observed strategy, here all energy reserved As residual reproductive value until Current benefit exceeds value of retention for later reproduction. Residual reproductive value Semelparous species

27. 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).

29. Evidence? • 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:

30. 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.