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Natural enemies complicate reproductive tradeoffs

Semelparous plants and animals are those that reproduce only once, whether after a few months of growth (annual plants, like wheat) or after years (“century plant� or most salmon). Iteroparous species iterate. That is, they reproduce repeatedly. For example, perennial grasses may produce seeds every year for a decade or more.

One reason this difference matters is that perennial crops may have some environmental benefits, relative to annual crops. Plowing, traditionally more common with annual than perennial crops, can greatly increase soil erosion, especially on steep slopes. So there is increasing interest in developing perennial grain crops as an alternative to wheat.

However, perennial plants have lower seed yield than their annual relatives, so we would need to devote more land to agriculture to get the same amount of grain. One reason for the yield difference is that an annual plant can transfer most of the carbon (energy) and nitrogen (needed for protein) from its leaves, stem, and roots into its seeds. It’s going to die anyway, so the next generation gets its accumulated wealth. A perennial plant needs to hold back some carbon and nitrogen for winter survival and spring regrowth. The more resources it puts into this year’s seed production, the less it can carry forward to support reproduction next year.

This week’s paper shows that iteroparous plants face additional costs when they reproduce, namely, ecological costs. “Herbivore-mediated ecological costs of reproduction shape the life history of an iteroparous plant� was written by Tom Miller and colleagues at the University of Nebraska (where I’ll be speaking on Darwinian Agriculture in April) and published in American Naturalist.

They studied the tree cholla cactus, Opuntia, which is eaten by the cactus bug, Narnia. This species produces new meristems (growing tips) each year, which become either seed-producing flowers or cladodes like very thick leaves, which contribute to future growth and reproduction by photosynthesizing. Thus, one simple measure of investment in current reproduction, perhaps at the expense of future reproduction, is the fraction of meristems that flower.

To measure the tradeoff between current and future reproduction, they injected a plant hormone, gibberellin into some Opuntia meristems, to prevent them from flowering. Control plants (injected too late to stop flowering) produced more flowers, as expected. They also attracted more bugs, which attacked the flowers. The more bugs, the more flowers aborted without producing seeds. They showed that this flower abortion was caused by the bugs, rather than being a side-effect of hormone treatment, because insecticide-sprayed plants had little flower abortion.

If the Opuntias make more flowers this year, they are trading potential seed production this year for future seed production. If, instead, they made more cladodes and fewer flowers, they would have higher photosynthetic rates next year to support more flower production. So far, this is similar to the tradeoff argument made previously against perennial grain crops. But this week’s paper shows that more flowers attract more bugs, so they don’t even achieve the potential benefit of greater seed production this year.

When they analyzed the tradeoffs between current and future reproduction based just on photosynthesis, they predicted that small plants should wait to flower until they are big enough to have a high photosynthetic rate, but big plants should have most of their new meristems flower. But when they included increasing bug damage with increased flowering, their model predicted that even large plants should have only about 60% of their meristems flower each year. This matches field observations for real plants. So apparently Optuntias (or rather the “blind watchmaker� of natural selection) have come to the same conclusion.
N. pallidicornis on flower bud.jpg
Narnia on Opuntia (photo from Tom Miller)

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