Plasticfruits, part 1: How an ordinary daisy becomes extraordinarily fruity

@chris_whitehouse @peterslingsby @lloyd_esler @adriaan_grobler @botaneek @graham_g @vynbos @troos @benjamin_walton @nicky @craigpeter @jon_sullivan @yvettevanwijk1941 @magdastlucia @joeysantore @alastairpotts @seanprivett @strandloper @arthur_chapman @fynbosphil @henrydelange @qgroom @carinalochner

I have noticed a principle in the biology of plants (https://journals.co.za/doi/abs/10.10520/EJC112757) that seems missing from textbooks.

Ponder the scientific implications of the observation that 'flower' (https://en.wikipedia.org/wiki/Flower) is less ambiguous than 'fruit' (https://en.wikipedia.org/wiki/Fruit).

The principle emerging from this is:
Flowers tend to be evolutionarily fixed, but fruits tend to be evolutionarily plastic.

This is why it is better to classify, and easier to identify, plants by their flowers than by their fruits.

It is also why the word 'flower' is less confusing, in botanical descriptions, than the word 'fruit'.

'Fruit' technically includes dry, dehiscent/ballistic pods and capsules, papery to woody follicles, and diverse other structures. These include compound structures incorporating calyces, peduncles, hypanthia, etc., and can contain from one seed to hundreds. However, 'fruit' is usually taken to mean something closer to the category of fruit in human diets.

Another way of saying this is that plants tend to be conservative in their sexual organs, but versatile in their organs of seed-dispersal. Or relatively fixed vs relatively modifiable. Fruits seem more adaptable than flowers within any given evolutionary lineage.

In this series of Posts, I focus on various examples of this principle at the level of genus (https://en.wikipedia.org/wiki/Genus).

So many genera, worldwide, illustrate the principle of 'plasticfruits' that my choices must be arbitrary. However, I would like to show diverse ways in which fruits have converged, evolutionarily in producing enough 'fleshiness' to provide edible rewards for seed-dispersing animals.

I start with simple - but surprising - examples, building to morphologically more complex examples.

My first choice is the daisy genus Osteospermum (https://en.wikipedia.org/wiki/Osteospermum), which occurs mainly in southern Africa.

The fruit in Osteospermum, as in other daisies (Asteraceae), is a cypsela (https://en.wikipedia.org/wiki/Asteraceae#Fruits_and_seeds) containing a single seed. It is often stated that daisies bear achenes but this is, strictly speaking, incorrect. A cypsela is similar to an achene but differs technically in the number of carpels (https://en.wikipedia.org/wiki/Gynoecium#Carpels).

It is the modification of the exocarp, or outer layer, of the cypsela that provides the main variation - which can be surprisingly eye-catching - in the fruits of various species of Osteospermum.

In some species, the cypsela bears three small wings plus an apical air-chamber, facilitating dispersal by wind. These species tend to occur in dry environments. I do not know whether the wings develop from the exocarp or from the calyx, but I suspect the former.

The fruit is this case would be described by most naturalists as a seed. It is actually a seed contained in the dead, dry carpels, but equates to a seed for practical purposes. (When you shuck a sunflower 'seed', discarding the hull to obtain the real seed inside, you are actually handling a whole fruit of Helianthus, https://en.wikipedia.org/wiki/Helianthus.)

In other species such as Osteospermum spinosum (https://www.inaturalist.org/taxa/591016-Osteospermum-spinosum and https://plants.jstor.org/compilation/osteospermum.spinosum), the cylindrical cypsela has no wing but its exocarp is thinly fleshy. This provides a meagre food-body designed to be eaten by ants as a reward for dispersal and sowing by these insects (https://journals.co.za/doi/pdf/10.10520/AJA00382353_2316 and https://www.researchgate.net/publication/222159641_Convergent_evolution_of_seed_dispersal_by_ants_and_phylogeny_and_biogeography_in_flowering_plants_A_global_survey).

The fleshy layer is thin and colourless, and not noticeable to the human eye. The fruit is not displayed but dropped to the ground immediately on ripening. If the fallen cypsela is not immediately collected by ants, the exocarp dries out and wrinkles within days or perhaps hours.

Here is another example: Osteospermum asperulum (https://www.inaturalist.org/taxa/61411-Osteospermum-asperulum). Also see https://www.sciencedirect.com/science/article/pii/S0254629915302970.

The structure described above is, again, a fruit in botanical terms but would not be described as such colloquially.

In yet other species, the cypsella is ribbed and/or pitted, or kidney-shaped, warty and pitted. The adaptive significance is unknown but this shows how variable the diaspores (https://en.wikipedia.org/wiki/Diaspore_%28botany%29) are within this single genus.

Finally, in a few species of Osteospermum the exocarp of the cypsela is fleshy enough to form something clearly recognisable as a fruit (https://www.inaturalist.org/observations/65954570) - and one that is perfectly edible for humans albeit too small and fiddly for most naturalists to bother with.

In these cases, the exocarp is thick and succulent enough to provide a jam-like reward to birds that swallow the whole cypsela, digest the sugary exocarp, and defecate or regurgitate the seed contained in it, which remains intact after digestion.

The cypsela in these cases not only conforms to the search-image for an edible, fleshy fruit, but changes in hue to present a pre-ripe display. The sequence, from green through yellow and red to blackish, flags to birds the imminent availability of the ripe, palatable exocarp.

The important point:
The flowers of all these species are similar, and unremarkable for daisies. Yet the fruits vary categorically in appearance and function, and this is achieved by evolutionary modification of a single part of the fruit: the exocarp.

If taxonomists were to use the fruits for classification, they would split Osteospermum into different genera. But what fits the evidence better is that this is one genus, with 'plasticfruits'.

The following illustrate the flower-heads, fruits and seeds of Osteospermum moniliferum (https://en.wikipedia.org/wiki/Chrysanthemoides_monilifera). This is dispersed mainly by birds but is one of the few species of daisies, worldwide, that presents fruit-flesh fully edible for humans.

In my experience, the fruits are best eaten when black, at which stage the fruit-pulp has changed from coherent/crisp to fluid. The taste is sweet with no sourness or astringency. I collect about 40 at a time in my mouth, burst them with my tongue one by one, swallow the jam, and spit out the seeds as I go along. I am hardly an agent of dispersal because my instinct is not to swallow the seeds, and I tend to linger at individual plants laden with fruit.

The sequence of colours is as follows. The nearly full-size, but still completely unripe fruits are leaf-green with a purple blush. The full-size but unripe fruits are dull yellowish green. The ripe fruits are brown. The fruit actually shrinks from the yellowish stage to the fully ripe stage, without wrinkling. The fruit-pulp seems to lose some bulk in the conversion from the turgid (still hardly sweet) fruit-pulp at the yellowish stage - which I find myself spitting out rather than eating it - to the ripe, jammy stage.

The following shows that the composite flower-heads are similar to those of thousands of species of daisies worldwide:
https://www.inaturalist.org/observations/71204410

The following show that a limited number of the flowers on each flower-head produce fruits, owing to constraints on space:
https://www.inaturalist.org/observations/71545076
https://www.inaturalist.org/observations/90427230
https://www.inaturalist.org/observations/76601465
https://www.inaturalist.org/observations/99457496
https://www.inaturalist.org/observations/62053603

The following show the development of hues in the pre-ripe display:
https://www.inaturalist.org/observations/100251297
https://www.inaturalist.org/observations/100486869
https://www.inaturalist.org/observations/99216334
https://www.inaturalist.org/observations/98605375
https://www.inaturalist.org/observations/98178097
https://www.inaturalist.org/observations/100865643
https://www.inaturalist.org/observations/99996133
https://www.inaturalist.org/observations/76086368
https://www.inaturalist.org/observations/76088858

The following show the fully-ripe fruits:
https://www.inaturalist.org/observations/100865707
https://www.inaturalist.org/observations/82152373
https://www.inaturalist.org/observations/100865570
https://www.inaturalist.org/observations/85178849

The following show the seeds divested of fruit-pulp by digestion or weathering:
https://www.inaturalist.org/observations/92064511
https://www.inaturalist.org/observations/57777300

to be continued...

Posted by milewski milewski, February 13, 2022 22:12

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https://www.sciencedirect.com/science/article/pii/S0254629915302970

https://pdf.sciencedirectassets.com/273500/1-s2.0-S0254629903X94004/1-s2.0-S0254629915302970/main.pdf?X-Amz-Security-Token=IQoJb3JpZ2luX2VjED8aCXVzLWVhc3QtMSJHMEUCIQD6geH7YUetNA%2Bu3OF%2BKRcRNjJjW%2FrGyJFYndvOI8w%2F9wIgfJA8QEV9omzddEQCp9tYQ1vOW4s79WJqVEQcZxNjN50qgwQIiP%2F%2F%2F%2F%2F%2F%2F%2F%2F%2FARAEGgwwNTkwMDM1NDY4NjUiDJna3LqP%2BYiqXrF96yrXAxYzIYlJli2r6IGe8Z91KCcrV47qairXOpUtLvpnizYqNAwznUSRv662XIojz%2Frf3cdFBAQcUr3V4VZGzKGs3gWCkhxyf9J%2FhFgg%2FhO3P%2Bp2pp5%2FumUH%2BoOF%2FnGPtbEBk%2BvJfCNMYPWIMqGDZvHrVZKNWJNVlYBJokcX%2FZbNg3mSBmu3vRtV5NFhx%2ByfzDOiuvBFY0wyNXMNmCVVDbrLeFaNTJ2AUodI%2FtE70b7GwtDloAMY16whZi0wkoeL8cO8ohHc1NL3fiw7UJqZtSJEz5Rm06%2BFWXhN4rTXHY6iLVcfjC72vL%2F3Pvnh98HfH1Pg5WpzbGCbUPMoSD6fBhMDWPfSJD2W33BZZ5XuDq1ShVdGnJQL2tdDahQpTgaX0rW0%2FY0BmBZgdzm%2FbuwTKz0k6Aui1FROuX8dhOQPMtljawKVz1KbJFQJHIgfKBy5LPY0xzH56iHMx974yAnZwjyaNlSIMd3kCILNGTdEGFJKeAwYIIa0zSvOzktyAWRbr4geWzF4Lx%2F5kfuFo2NjpgsarAzjCv0RUPOGIfDz8%2Fm%2FFVLbav4xJyHSCV%2FgCQtj45uarAS7Q3ni%2BbOusfx3mUrO0z7hRiQTlWM1xOC1gbUHMlK0zu0MrvP83zD686eQBjqlAa%2BnGti1xksd%2Bd6zH2aB5ds4VC%2B8p6V0r4O%2FAp6i2AZ0IRTKrOjCeISJ5KYKb94kC8518ftHW2BjT7xcBlI3DQaLWqzF1845hGCWDnSV3F5OKMgEppzs10XUkV4CBRX8TjuC65Q1SrB7qP%2FOVTnes5PdIiXiaJcOzYJhdaLks%2F541cLkgZPtBtYFphRJUXdxu4jBYJ6hyIAG0Tmq%2BXwbYUS9KAaaVQ%3D%3D&X-Amz-Algorithm=AWS4-HMAC-SHA256&X-Amz-Date=20220214T075941Z&X-Amz-SignedHeaders=host&X-Amz-Expires=300&X-Amz-Credential=ASIAQ3PHCVTYRWXLMK3F%2F20220214%2Fus-east-1%2Fs3%2Faws4_request&X-Amz-Signature=d4bcfa7f3d1f1ae68cca3c28291e6d1fbb1d01ae5b1a378e0f23b597f63dcc48&hash=d0f0994b9212aa3f4b48faeac554362f1bee3ca3d2d1838a748afd180019806c&host=68042c943591013ac2b2430a89b270f6af2c76d8dfd086a07176afe7c76c2c61&pii=S0254629915302970&tid=spdf-add08407-1a0e-49b2-8eba-858bf72edf03&sid=75f892373843f84f476a1e9271b873959507gxrqa&type=client&ua=5000015b055252025759&rr=6dd4c22c79ca17c7

Posted by milewski 8 months ago (Flag)

Leucopogon, a genus belonging to a different family (Ericaceae), partially parallels Osteospermum in its range of categories of dispersal. Many species are dispersed and sown by ants (e.g. https://en.wikipedia.org/wiki/Leucopogon_amplexicaulis#:~:text=regenerates%20by%20seed.-,The%20seeds%20are%20thought%20to%20possibly%20be%20dispersed%20by%20ants,enriched%20and%20well%2Ddrained%20soil) while a few species have colourful fleshy fruits attractive to birds (e.g. https://www.inaturalist.org/observations/105690319 and https://www.inaturalist.org/observations/103940509 and https://www.inaturalist.org/observations/105188527 and https://www.inaturalist.org/observations/68195869 and https://www.inaturalist.org/observations/105600747).

In Leucopogon the fruit is a drupe, not a cypsela.

The parallel with Osteospermum may be only partial because I do not know if any species of Leucopogon is adapted mainly for dispersal by wind.

A particularly remarkable genus of Ericaceae, w.r.t. 'plasticfruits', is Gaultheria: https://botanicallyinclined.org/gaultheria-procumbens-fruit-revealed/2021/.

Posted by milewski 8 months ago (Flag)

I wonder if one should not include humans as dispersal animals!? They have been around for 100.s of thousands of years and been eating and spitting out or otherwise dispersing seeds through all that time. Also they have migrated all over the worls and have moved species or helped in speciation and also evolution by choosing the largest sweetest fruits to eat? I would love someone to take this up as a research project, the human element in dispersal and evolution of plants through time/

Posted by yvettevanwijk1941 8 months ago (Flag)

@yvettevanwijk1941 Hi Yvette, Many thanks for these thoughts. It would indeed be good to investigate systematically which species of wild plants in southern Africa were dispersed and sown by hunter-gatherers. I doubt that Osteospermum moniliferum was among them, because a) in my experience one does not ingest the seeds (this seems instinctive), and b) the fruits are unlikely to be transported back to camp for consumption, because they are perishable, fiddly and messy. So I see humans as detracting from dispersal rather than contributing to it, in this case. Your further thoughts?

Posted by milewski 8 months ago (Flag)

Just that spitting seeds out still disperses them!? These small Boetabessies would probably be eaten as snacks in passing, and by kids playing, but as mentioned above one sucks them and then spits out the seeds which might mean seeding them some distance away from the parent plant. Also Hunter-gatheres might not have been as averse to swallowing small seeds as we are today.

Posted by yvettevanwijk1941 8 months ago (Flag)

@yvettevanwijk1941 I agree to some extent, because what I noticed when eating the fruits of Osteospermum moniliferum is as follows.

Firstly, the skin of the ripe fruit is strong enough (despite the softening of the fruit-pulp to a jammy consistency) that I need to pinch the fruit between tongue and incisors to burst the fruit. This takes a small amount of time. It takes me a few minutes to mouth-mash and mouth-process a big mouthful (more than 40 ripe fruits), spitting the seeds out as I go along.

However, please bear in mind that when one finds a stand of individual plants laden with fruits, one tends to remain for mouthful after mouthful, which means that most of the seeds are spat close to the source.

Secondly, I have noted that the feces of Papio ursinus ursinus (e.g. near Hermanus in October 2002) are full of the seeds after this species has eaten the fruits of Osteospermum moniliferum. This is puzzling because the seeds are big enough that my instinct is certainly not to swallow them; the mouth of P. ursinus is smaller than the human mouth, so I would have expected that species to be even more reluctant to swallow the seeds. Yet it swallows them wholesale, apparently without crushing many of them in its jaws (although we need more observations to confirm that the seeds are viable after being defecated by P. ursinus).

So it seems that human and baboon are different as dispersers of O. moniliferum, but I don't know which species is the more effective disperser. Humans certainly spit out the seeds in viable condition, but the distances they are transported are limited. Baboons transport the seeds far, but possibly harm them by chewing or digestion.

Posted by milewski 6 months ago (Flag)

Osteospermum moniliferum was fully in fruit at Rhodes Memorial, next to the University of Cape Town, in early November 2002. At this time I noticed many instances of the seeds among the buildings on campus (including window-sills just inside buildings), where they had been regurgitated by Onychognathus morio (https://www.inaturalist.org/taxa/204554-Onychognathus-morio) during the breeding season of this species. The regurgitated 'pellets' consisted of several seeds encased in a dark, fibrous material that I assume to be the fruit-skins. On the ground at the base of a roost and/or nest of O. morio on one of the buildings on campus, I found dozens of clean seeds of O. moniliferum, probably also regurgitated. I do not know whether the parents were feeding the fruits of O. moniliferum to their nestlings or not.

Posted by milewski 6 months ago (Flag)

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