Why would phylicas mimic fleshy fruits?

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Phylicas (Phylica https://inaturalist.ala.org.au/taxa/185032-Phylica and Trichocephalus https://www.inaturalist.org/observations?taxon_id=567637) are, in most ways, unremarkable heath-like shrubs.

Their 'ericoid' (https://en.wikipedia.org/wiki/Ericoid) growth-forms are convergent with many other families and genera in the various heathlands of the world, from Scandinavia (https://gfmc.online/wp-content/uploads/06-IFFN-38-Kvamme-Norway-2.pdf) to southernmost Australia (https://www.awe.gov.au/sites/default/files/documents/mvg18-nvis-heathlands.pdf).

Similar-looking evergreen plants with small, dull-coloured leaves have repeatedly evolved in Ericaceae, Myrtaceae, Asteraceae, Rutaceae, Thymelaeaceae, Rosaceae, Lamiaceae, Fabaceae, Polygalaceae and Bruniaceae. And it is after these various heath-like plants that a whole category of vegetation in South Africa, fynbos (https://en.wikipedia.org/wiki/Fynbos), is named.

Furthermore, the convergence extends to modes of dispersal and sowing. Many species, in phylicas and many other genera of heath-like plants, participate in a syndrome called myrmecochory (https://en.wikipedia.org/wiki/Myrmecochory), in which the fruits are dry capsules and the seeds, once shed to the ground, are collected and buried by ants (https://journals.co.za/doi/pdf/10.10520/AJA00423203_1083).

Where phylicas are unusual is that, in perhaps twenty species, the immature capsules have such conspicuous yellowish and reddish hues that at first glance they seem to mimic fleshy fruits attractive to seed-dispersing, frugivorous birds.

This similarity is deceptive. Not only are the fruits of our phylicas in no sense 'ripe' while they are bright-hued, but no species of phylica

is bright-hued when actually mature ('ripe').
is known to be disseminated by frugivorous birds, or
actually possesses fleshy fruits.

As the fruits of our phylicas develop, they turn from inconspicuous green (growing) through conspicuous red/yellow (full-size but still immature) to inconspicuous brown (mature). This means that at the stage when the capsules have conspicuous hues, the seeds are not yet ready for dispersal.

The conspicuousness of the hues of the immature capsules of our phylicas is puzzling. This is because:

few other heath-like plants, anywhere on Earth, show a similar pattern,
there seems to be no adaptive benefit to attracting attention to the immature fruits,
the colourful conspicuousness is not accompanied by the palatability to birds that is expected in fleshy fruits, and
it is consequently unlikely that a mutualistic interaction between plants and animals is involved.

Although the transitionally bright hues would seem to constitute a 'pre-ripe display', this makes little sense.

Such a display can hardly be aimed at the seed-dispersing ants (e.g. Anoplolepis, Pheidole and Camponotus, https://www.proteaatlas.org.za/antarg.htm and https://journals.co.za/doi/pdf/10.10520/AJA00423203_1083). This is because:

most ants are probably insensitive to red (https://wildaboutants.com/2010/04/01/ant-color-vision/ and https://myrmecologicalnews.org/cms/index.php?option=com_download&view=download&filename=volume10/mn10_41-50_printable.pdf&format=raw and https://www.researchgate.net/publication/323567457_Spectral_sensitivies_of_ants_-_a_review),
even if ants see red, the distance from the ground to the crown of the shrub makes it unlikely that the display would be efficient, and
ants have not been observed to climb the plants to extract the diaspores from the capsules; instead they wait until the capsules have dehisced and the diaspores have been shed to the ground.

What all of this means is that the conspicuousness of the immature capsules of our phylicas is more likely to function as 'warning colouration' (see http://www.esalq.usp.br/lepse/imgs/conteudo_thumb/Defensive-Coloration-in-Plants-A-Review-of-Current-Ideas-about-Anti-Herbivore-Coloration-Strategies.pdf) than as attractive colouration.

If so, which animals are being warned, and which defensive capacity is being advertised?

The only relevant animals are diurnal birds and anthropoid primates, both of which have eyes sensitive to red. And any defensive capacity being advertised seems likely to be chemical.

Seed-eating finches (Serinus, https://en.wikipedia.org/wiki/Serinus) are common in fynbos vegetation and are likely to eat the diaspores of our phylicas when available. However, they have not been recorded attempting to open the immature capsules. Furthermore, even if they did, it is hard to see how noxious/toxic chemical substances in the capsule-walls would deter them, given that the finches need not ingest these.

This leaves the chacma baboon (Papio ursinus, https://en.wikipedia.org/wiki/Chacma_baboon) - which was formerly widespread in the habitats of phylicas and remains present with many species - as a plausible agent.

Baboons routinely eat immature fruits of various types of plants to digest the seeds within. Where the fruits are too small to be handled efficiently, no attempt is made to extract seeds one by one. Instead the whole capsule of e.g. phylicas would be chewed up, destroying many/most of the seeds.

No toxic substance has been recorded in the immature capsule-walls of phylicas. But this could simply be because nobody has investigated this.

There are about 150 species of phylicas, making generalisations risky. However, there are at least two indications that our phylicas are particularly vulnerable to 'pre-dispersal seed-predation', as follows:

the fruits seem to take longer to develop than in various other plants in fynbos, and
even when the capsules have matured, they tend to dehisce tardily (an extreme example seems to be https://www.inaturalist.org/observations/103369067 and https://www.inaturalist.org/observations/62883570).

The tardy dehiscence in phylicas suggests that at least some of the species are 'semi-serotinous' (see https://en.wikipedia.org/wiki/Serotiny and https://eurekamag.com/research/004/873/004873786.php and https://www.publish.csiro.au/bt/bt14237). If so, the seeds tend to be retained safely in the crown for months, rather than being released.

So here is a hypothesis.

In our phylicas, a substance toxic to the chacma baboon is synthesised in the developing capsules. This substance does not necessarily have a repulsive taste, but it poisons the consumer soon enough after eating that a negative association results. The bright hues reinforce the message and serve as a reminder discouraging subsequent consumption.

This hypothesis can be tested by:

chemically analysing the immature capsule-walls of several species,
personally experimenting by chewing small quantities of the bright-hued, immature capsule-walls,
offering freshly-plucked immature vs mature capsules vs diaspores to wild populations of the chacma baboon in cafeteria experiments.

The following observations in iNaturalist nicely illustrate the bright hues but await identification: https://www.inaturalist.org/observations/11204217 and https://www.inaturalist.org/observations/101625096 and https://www.inaturalist.org/observations/105862753 and https://www.inaturalist.org/observations/93693260.

The following, in alphabetical order of species, illustrate some of the identified phylicas in which the immature capsules have puzzlingly bright hues.

Phylica cylindrica https://www.inaturalist.org/taxa/591989-Phylica-cylindrica and https://www.inaturalist.org/observations/35732494 and https://www.inaturalist.org/observations/16544546 and https://www.inaturalist.org/observations/35144591 and https://www.inaturalist.org/observations/63303724

Phylica ericoides https://www.inaturalist.org/taxa/470408-Phylica-ericoides and https://www.inaturalist.org/observations/98995567 and https://www.inaturalist.org/observations/61143551 and https://www.inaturalist.org/observations/57113679 and https://www.inaturalist.org/observations/52680449 and https://www.inaturalist.org/observations/23942932 and https://www.inaturalist.org/observations/11192570

Phylica oleifolia https://www.inaturalist.org/taxa/567693-Phylica-oleifolia and https://www.inaturalist.org/observations/94453801 and https://www.inaturalist.org/observations/97343683 and https://www.inaturalist.org/observations/94689300 and https://www.inaturalist.org/observations/93987380

Phylica rogersii https://www.inaturalist.org/taxa/592058-Phylica-rogersii and https://www.inaturalist.org/observations/11226056 and https://www.inaturalist.org/observations/41376418

Phylica spicata https://www.inaturalist.org/taxa/592065-Phylica-spicata and https://www.inaturalist.org/observations/35853738

Phylica velutina https://www.inaturalist.org/taxa/578029-Phylica-velutina and https://www.inaturalist.org/observations/8851341 and https://www.inaturalist.org/observations/8851343 and https://www.inaturalist.org/observations/11253556 and https://www.inaturalist.org/observations/11284287

Phylica villosa https://www.inaturalist.org/observations/93557841

Trichocephalus stipularis https://www.inaturalist.org/taxa/567636-Trichocephalus-stipularis and https://www.inaturalist.org/observations/61424103 and https://www.inaturalist.org/observations/61082239 and https://www.inaturalist.org/observations/99961494 and https://www.inaturalist.org/observations/99444544

Posted on February 26, 2022 04:00 AM by