Tītoki and other New Zealand sexy plants

One of the peculiarities of New Zealand plants is the high proportion of them, among seed plants at least, that separate male and female sexual functions onto different plants.  Humans and most familiar animals do this too, so it seems to most people to be normal that there should be males and females in all organisms.  But most plants are cosexual; that is, there's only one kind of individual in a population, and it has both male and female reproductive functions.

Veronica decora (here at Moke Creek, Otago) is cosexual; every plant produces both pollen and ovules, in this case in hermaphrodite flowers.

In gender dimorphic plants—those that have two sexes—it's not always a straight-forward issue of being either male or female though.  When plants are either strictly male—producing pollen and no ovules—or strictly female—producing ovules but no pollen—the population is called dioecious.  But in many dimorphic plants, male individuals can also produce ovules and even set some fruits and seeds, a condition called gynodioecy.  Usually the males vary in their seed production, with most producing none or very few, and then a continuous range all the way up to a few plants that may produce quite a lot.  David Lloyd pioneered a method to quantify this variability in maleness and femaleness (it works for cosexual plants too), which helps greatly in visualising, describing, and ultimately understanding plant sexuality.

Female (left, cultivated) and male (right,  Makara Peak) of Aciphylla squarrosa.

New Zealand and a few other places, like Hawai'i, have a high percentage of species where there are separate male and female plants.  Maybe that's because genera like Aciphylla (above) and Coprosma, where all the species are separate-sexed, have undergone radiations here leading to large numbers of species.  But you can correct for that somewhat by using the genus as a measure: have we got more genera with separate sexes than other parts of the world do?

Colin Webb, David Lloyd, and Lynda Delph asked this question back in 1999 (free download here).  They calculated we have 83 seed-plant genera—23% of the genera in the flora—in which at least some species have separated sexes, and that's very high by international standards.  Since then a few more genera have been added to the list, like Teucridium, Toronia, and Corynocarpus (free downloads here, here, and here), but taxonomic changes have reduced the number a bit too, so the estimate is still probably about right.

Given this unusual feature of the flora, it's perhaps not surprising that New Zealand has produced a number of internationally recognised researchers of plant reproductive biology, headed of course by David Lloyd (1937–2006).  I've been aware for a while that nearly all of them did their research in the South Island, and we know that (roughly speaking) in New Zealand tree diversity decreases with increasing latitude, while alpine plant diversity increases.  So it's not surprising perhaps that the newly-discovered instances of separate-sexed genera are mostly northern and two are trees.  There might even be a few more waiting to be noticed; I've got my eye on another genus at the moment.

The variability of sexual systems in some genera, again often northern, still might not be fully described.  Kohekohe (Dysoxylum spectabile) and tītoki (Alectryon excelsus) were listed by Webb et al. as dioecious, but they need close examination to check for gynodioecy.  In kohekohe, a few fruits can be found on some male trees, and I've seen a few fruits on male tītoki, at least in cultivated trees.

Kohekohe (Dysoxylum spectabile), fruits on a female tree.

I'm sorry; I didn't start out to write such a long introduction to what's only a quick observation and a couple of photos.  But it's necessary to set the scene.  Yesterday I went to look at a large population of tītoki in flower at Waiorongomai, near lake Wairarapa.  Here, scattered tītoki trees persist in a grazed paddock on a small area of alluvial river flats, along with some rewarewa and mataī trees.  The lower branches of the tītoki are often within reach, making their study possible.  So I was hoping to check out what their flowers are like, and maybe to observe old fruit on some male trees.

There were obviously two sorts of trees in this population: those that were covered in fruit and those that weren't.  Clearly, last year's flowering had produced a bumper crop.  The trees that weren't bearing fruit were also flowering, and every one that I could reach was a male; the flowers had usually eight stamens and masses of pollen.

Tītoki, male flower.

The fruiting plants weren't flowering, except for one that had a couple of small flowering branchlets within reach.  The flowers on these were different: they had a larger ovary and an obvious red stigma.  But they also had stamens that appeared to be of normal size.  None of the anthers had opened, and I've yet to check (next time I'm near a compound microscope) if they contain pollen.  My expectation is that if they do contain pollen it'll be sterile or maybe have no pores to germinate through, but I could be wrong.  In other words, this observation doesn't really help answer whether tītoki is dioecious or gynodioecious.

Tītoki, female (or maybe hermaphrodite?) flower

Why is it that only the males (with one exception that barely counts) are flowering this year?  It seems counter-productive for males to flower when there are no eggs available to be fertilised.  My hunch is that last year was such a prodigious flowering and fruiting that the female trees have to take a rest; they've been investing their resources in fruit production all through 2012, and that's much less risky than investing in flowers that are only potential fruits.  Males haven't had that costly investment to bear, so they can afford to flower again.  And they have no way of knowing whether the females are flowering or not.

Also, for a male it's a good evolutionary strategy to have sex whenever you can (I always tell my students that biological truth—a consequence of Bateman's Principle—doesn't make it morally or socially acceptable though; we're talking about trees here, not sentient social animals that have to live in a society).  Male flowers and pollen are cheap to produce, so even if most of them might be wasted it's a risk that's worth taking.  This year, pollen from all those male flowers will be competing for the few flowers on that one female tree and next year I'd expect to see very few fruits available in this population.  Unless, that is, some of those male trees can make some fruits, in other words if this population is gynodioecious.

Tītoki, fruit.  The black shiny seed is surrounded by a fleshy aril that attracts birds.

Time will tell, and a revisit is already in my diary for November 2013.  Ideally there'll be a student, interested in making a study of tītoki sex into an honours project, to do the hard yards of all that counting and measuring.

Update, added 26 November 2012.

One of my undergraduate students read the blog above and immediately went to check trees in her mother's garden (in Waikato, North Island).  She sent the photo below, which she correctly described as an inflorescence with mostly male but a few female flowers.  That fits well with my observation that some male trees can set a few fruits, and suggests pretty strongly that tītoki is gynodioecious (we still need good population samples to be sure and to describe the system in detail).

Tītoki inflorescence with male flowers and a few female ones (two are circled)

This observation is also consistent with the comment by Webb et al. (1999) that dioecy in tītoki (probably gynodioecy, we now know) evolved from monoecy, presumably because its relatives are monoecious.  In monoecious populations, all plants are cosexual, and they have separate male and female flowers.  From monoecy, a mutation that suppresses maleness can spread in the population to produce a proportion of female-only plants.  The plants that retain both male and female flowers now reproduce mostly as males because only they can pollinate all the female flowers in the population, their own and all the flowers on the females; that why we call them male now.  Often they come to specialise and some or most may become specialist (constant) males, which seems to be the case in tītoki.  If they all become constant males, the population has moved all the way to dioecy.

You might ask how I can be confident the photo above shows a male with a few female flowers, rather than a female with a few male flowers.  Populations with constant males and inconstant females (females that can produce some pollen) are called androdioecious.  It's an exceedingly rare sexual system and seems to need some special conditions in order to evolve and persist.  There are only a few well-documented examples.  So, given that gynodioecy is vastly commoner, and also that most of the flowers on this branch are male while only a few are female, I think that gynodioecy is the most likely sexual system in tītoki.

References

Webb, C., Lloyd, D., & Delph, L. (1999). Gender dimorphism in indigenous New Zealand seed plants New Zealand Journal of Botany, 37 (1), 119-130 DOI: 10.1080/0028825X.1999.9512618

Lloyd, D. (1980). Sexual strategies in plants III. A quantitative method for describing the gender of plants New Zealand Journal of Botany, 18 (1), 103-108 DOI: 10.1080/0028825X.1980.10427235