What is the adaptive value of yellow hue in the fruits of Euphorbia damarana?

@robertarcher397 @alexdreyer @peter_erb @tonyrebelo @jeremygilmore @ludwig_muller @troos @botaneek @nathantaylor @duch @pieterwinter @jrebman

Euphorbia (https://en.wikipedia.org/wiki/Euphorbia) is an extremely large and widespread genus, with a range of growth-forms.

The following show various mechanisms of seed-dispersal in Euphorbia: http://xavierespadaler.creaf.cat/Archivos/1990s/1991/BotChron10_697-705.pdf and https://d1wqtxts1xzle7.cloudfront.net/41748277/510-libre.pdf?1454099700=&response-content-disposition=inline%3B+filename%3DExplosive_seed_dispersal_in_two_perennia.pdf&Expires=1666821668&Signature=V3JoMwWOreTnRp9Ue7PLn8JrHG5dHpCXOGmlPhfhU0SUA~wWgwEislkPt7FEDv-s6eVqfPV~nKKEqjCZbzJtAoh61EvvlJYw-2z9VMMSS8iZzeIjxwd3e8ZcglcKt9HcSvS53V70g4fxFSYvTWQD-qwqo35HUd6SMP~5UBLdkD4sAYexB4D7K2fgd-Zb5QHVZbe83AZ7iI~AofZ8TRrXS6qRBTrCC48MuPHY~pWCWGDzYcMe~f7PDoxcBckM9ypy8C5w-gWDwPFeoH36BJbEj6v-URajrXkYOsMtA34NwxuVTygA3lF0wWFINArkhAEIsgDdDahaAuhE5UYtYUzXQw__&Key-Pair-Id=APKAJLOHF5GGSLRBV4ZA and https://pubmed.ncbi.nlm.nih.gov/21652429/ and https://www.jstor.org/stable/4123900 and https://www.researchgate.net/publication/257933870_Seed_dispersal_in_West_Mediterranean_Euphorbia_L and https://www.researchgate.net/publication/232680531_Pollination_and_Seed_Dispersal_in_the_Endangered_Succulent_Euphorbia_brevitorta and https://bioone.org/journals/journal-of-east-african-natural-history/volume-99/issue-1/028.099.0104/Pollination-and-Seed-Dispersal-in-the-Endangered-Succulent-Euphorbia-brevitorta/10.2982/028.099.0104.short.

Most spp. have dehiscent capsules (in some cases ballistic), with the dispersed seeds then tending to be sown by ants.

However, Euphorbia damarana (https://www.shutterstock.com/editorial/image-editorial/dry-open-landscape-damara-milk-bush-melkbos-euphorbia-3720916a and https://www.inaturalist.org/taxa/524175-Euphorbia-damarana and https://www.guenther-eichhorn.com//namibia_nature.html and https://www.kakteenforum.com/t28712-euphorbia-damarana) seems to be an exception.

This is a dull-green, toxic, leafless, drought-tolerant shrub. It is restricted to northwestern Namibia, where it dominates the vegetation over considerable areas, on basaltic, stony ground.

Euphorbia damarana is one of several superficially similar spp. of its genus in southern Africa and Madagascar (see https://www.inaturalist.org/taxa/568122-Euphorbia-burmannii and https://www.inaturalist.org/taxa/401782-Euphorbia-mauritanica and https://www.inaturalist.org/taxa/569116-Euphorbia-rhombifolia and https://www.inaturalist.org/taxa/524578-Euphorbia-tenax and https://www.inaturalist.org/taxa/585669-Euphorbia-stolonifera and https://www.inaturalist.org/taxa/429366-Euphorbia-alluaudii-oncoclada).

However, what is obvious from photos is that the habitat of E. damarana is extremely rich in large mammals, particularly considering the semi-arid climate. The species include Loxodonta africana, Diceros bicornis, Equus hartmannae, Giraffa giraffa, Strepsiceros strepsiceros, Oryx gazella, Antidorcas marsupialis, and Raphicerus campestris.

For illustrations of some of the above, in association with E. damarana, please see https://www.stevebloom.com/index.php?page=single&id=510386-BS1 and https://wilderness-safaris.com/our-camps/countries/namibia/guided-explorations/desert-oases and https://www.agefotostock.com/age/en/details-photo/black-rhino-desert-rhino-camp-palmwag-concession-damaraland-namibia-africa/YY9-2568226 and https://artofsafari.travel/wp-content/uploads/2017/02/Namibia_Damaraland_SkeletonCoast_WildernessSafaris_DesertRhinoCamp_TrackingBlackRhinoOnFoot1.jpg and https://www.shutterstock.com/image-photo/namibia-wild-giraffes-damaraland-region-1515147866 and https://www.shutterstock.com/image-photo/rare-endangered-hartmanns-zebra-mountain-damaraland-1112271035 and https://www.agefotostock.com/age/en/details-photo/giraffe-in-damaraland-three-young-giraffe-with-her-mother-africa-namibia-giraffenfamilie-im-damaraland-drei-junge-giraffen-mit-mutter-afrika-namibia/VIG-584253 and https://www.alamy.com/an-oryx-antelope-standing-in-the-stone-desert-of-namibia-image442698732.html?imageid=67B1F953-2958-455A-B6E0-C863C884B783&p=1376036&pn=1&searchId=f09f8f636935611f546ac96f8c12a0e4&searchtype=0 and https://www.desertlion.info/data/images/1/4/6/fem1euph.jpg and scroll in https://www.firstlightworkshop.com/namibia-2020-photo-tour/.

These associations make it particularly intriguing that the fruits of E. damarana are yellow (https://www.inaturalist.org/observations/10969800 and https://upload.wikimedia.org/wikipedia/commons/6/67/Euphorbia_damarana_2_MHNT.JPG and https://www.flickr.com/photos/verticalplanar/3929203798).

This hue is bright enough for there to be a superficial resemblance to fleshy fruits, edible to seed-dispersing birds and mammals.

My attention was first drawn to E. damarana when I watched a documentary made by BBC in April-May 1998. The footage and narrative portrayed the hook-lipped rhino (Diceros bicornis) as eating the fruits of E. damarana, and defecating intact seeds.

Apparently, this filming was done at the boundary of the Skeleton Coast National Park (https://en.wikipedia.org/wiki/Skeleton_Coast_National_Park), west of Palmwag (https://en.wikipedia.org/wiki/Palmwag).

To give readers an idea of how odd the fruits of E. damarana are, please note the contrast with e.g. E. mauritanica, which is common elsewhere within the historical distribution of the hook-lipped rhino.

In iNaturalist, there are currently 1,862 observations of E. mauritanica, but none of these shows fully-formed fruits. This indicates that, in this species, the capsules dehisce and disintegrate immediately on reaching full size, shortly after flowering.

So, about two decades ago, I investigated this unusual case of yellow, somewhat persistent fruits in E. damarana. I wrote to three persons (two of them since deceased) who had lived and worked in its habitat.

This correspondence confirmed that the fruits are similar to those of other spp. of Euphorbia in being dehiscent capsules, i.e. they are not fleshy. However, they are tardily dehiscent, the implication being that the still-attached capsules remain sealed (and attractively yellow) for an anomalously long time for the genus Euphorbia.

The strongest case for dispersal by mammals was made by the late Blythe Loutit (https://en.wikipedia.org/wiki/Blythe_Loutit). She replied to me, on 19 February 2003, as follows:

"To confirm that the fruit of Euphorbia damarana is fleshy and remains intact (as opposed to dehiscing), black rhino, ground squirrel, kudu and elephant have been observed eating the fruit. The most interesting are the ground squirrel, which climb up the finger-like branches to collect the fruit only when these are ripe, yellow/ochre. This method of dispersal may account for these euphorbias forming communities where ground squirrels are actively taking them into the burrows and literally planting as well as harvesting."

The late Mike Hearn (https://www.theguardian.com/environment/2005/feb/25/guardianobituaries.conservationandendangeredspecies) replied to me, around the same time, as follows:

"Black rhino do feed on the yellow fruit of Euphorbia damarana, as do kudu and oryx. Elephant have been observed feeding on the roots of the euphorbia. Kudu and oryx do feed on the new shoots of the euphorbia, but only the rhino feeds on Euphorbia damarana in significantly large quantities of new and old growth. Rhino also feed on Euphorbia virosa, sometimes consuming almost the entire bush, which can stand at > 1 m high. I hope to explore the issue of rhino as a disperser of some of the Namib Desert plant species in a chapter of my PhD, much in the same way Leader-Williams did with Kigelia in Zambia."

Patricia Craven (https://herbaria.plants.ox.ac.uk/bol/Content/Projects/namibia/Resources/PublicationsbyPatriciaCraven.pdf) replied in December 2002, informing me that favourite foods of the hook-lipped rhino in the area where the BBC did their filming are Tetraena simplex (https://www.inaturalist.org/taxa/595215-Tetraena-simplex) and Merremia (https://www.inaturalist.org/observations?place_id=7140&taxon_id=53440&view=species). She suggested that these foods were perhaps unavailable at the time when the documentary was made, causing the hook-lipped rhino to turn to E. damarana more than usual.

She continued:

"They may have eaten the fruits because they were hard up, but I think more likely the rhino were more interested in the stem tips and ate the fruits at the same time. After rain, the fibrous stems grow fast (quite a few cm) and also have leaves fleetingly. They are tough, but not woody. The late 90's were good rain years in most of the north-west and the rhino were also able to move far west into the real desert where vegetation is more scarce. From my experience rhino do eat the stems and the nutritional value was provided in Madoqua 1987 vol. 15(1)."

(See https://journals.co.za/doi/pdf/10.10520/AJA10115498_538.)

Patricia Craven's reply continued as follows:

"I feel sure that Blythe Loutit would have mentioned the seeds (of Euphorbia damarana), or had them evaluated, if they were seen to be important. However, the decade in which her work was carried out was exceptionally dry, and fruiting was not an annual occurrence, if I remember correctly. Euphorbia damarana was previously included in E. gregaria which is found in southern Namibia. Rhino did occur there many, many hears ago, but there are no records of what they may have eaten. See paper on 3 related spp., Bothalia 11(4), 500, in about 1974. Euphorbia damarana fruit does eventually dehisce, but is TARDY. It has been suggested that this is an adaptation to prolonged drought. The fruit is not really fleshy. The fruits have a very thin fleshy outer covering and a woody interior. The fleshy part dries very quickly, and the word 'fleshy' is relative. I would say it is hard and never soft like a 'true' fleshy fruit. The fruits definitely dry out in the bush and are not carried off intact. I would think they are a bit large for most of the desert animals to carry intact. I do not think it is bright enough to attract birds. In its environment, the ripe fruits of E. damarana are noticeable from a distance, but generally a dullish yellow. Maybe lighting played a part (in making them conspicuous in the BBC documentary footage), but I think they were photographed when very fresh, when for a short period they may be considered yellow. When the fruits of E. damarana dehisce, the seeds fall to the ground, and are eaten by rodents. Their paths are noticeable between the different bushes. I am not sure which species of rodents eat these seeds. We were intrigued to find out if the seeds were not as poisonous as the rest of the plant, or if the rodents were just able to cope with the toxins. I barely survived one seed!! I also have noted that the previous season's seeds (black) were still present with fresh seeds (green-yellow), so they are not all eaten. We have seen the remains of chewed stems still on the bushes and also removed. I think these were generally only noticeable in very dry periods. The parasitic Hydnora is found on its roots and is utilised by JACKAL and other animals."

(Please see https://www.inaturalist.org/observations/122554763.)

DISCUSSION

The yellow hue and tardiness of dehiscence of the fruits of E. damarana remain unexplained, in adaptive terms.

The role of the hook-lipped rhino (Diceros bicornis), although played up by a BBC documentary nearly a quarter of a century ago, remains questionable in terms of any mutualism involving seed-dispersal.

It remains plausible that E. damarana

• is dispersed and sown by ground squirrels (Geosciurus inauris, https://www.inaturalist.org/taxa/871614-Geosciurus-inauris, and/or Geosciurus princeps, https://www.inaturalist.org/taxa/871613-Geosciurus-princeps), and
• is the only species of Euphorbia adapted to squirrels (Sciuridae) for seed-dispersal.

Regardless, there seems to be no real analogy with fleshy fruits (whether yellow or any other hue/tone). This is because it seems unlikely that the yellow structure itself (i.e. the capsule wall) embodies any food-reward dedicated to consumers. Furthermore, the mystery remains of how any mutualism could have evolved without reduction of the toxicity of the seeds in E. damarana.

In summary, the dispersal biology of E. damarana deserves further investigation. The central question remains: if the plant is advertising its fruits to certain animals, which are the animal spp. involved, and what is the benefit to the plant?

Posted on October 26, 2022 08:15 AM by milewski