Today we have a long and edifying photo-and-story contribution from Athayde Tonhasca Júnior. His narrative is indented, and you can enlarge his pictures by clicking on them.
- Together, for better or worse
In 1844, Captain John C. Frémont of the US Army Corps of Engineers, later a US Senator and Governor, was crossing the Mojave Desert when he came across a Joshua tree (Yucca brevifolia), hitherto unknown to white settlers. In his report, the captain offered a harsh appraisal of his findings: “Associated with the idea of barren sands, their stiff and ungraceful form makes them to the traveler the most repulsive tree in the vegetable kingdom”. But Frémont was moderate when compared to Joseph Smeaton Chase, author of California Desert Trails (1919): “It is a weird menacing object more like some conception of Poe’s or Doré’s than any work of wholesome Mother Nature. One can scarcely find a term of ugliness that is not apt for this plant. A misshapen pirate with belt boots hands and teeth stuck full of daggers is as near as I can come to a human analogy. The wood is a harsh, rasping fibre; knife blades long hard and keen fill the place of leaves; the flower is greenish white and ill smelling; and the fruit a cluster of nubbly pods, bitter and useless. A landscape filled with Joshua trees has a nightmare effect even in broad daylight: at the witching hour it can be almost infernal”.
Joshua trees © Joshua Tree National Park, Wikimedia Commons:
Frémont’s and Smeaton Chase’s unfavourable aesthetic appraisals are not widely shared: many gardeners and landscapers like the peculiar shapes and looks of yuccas or palm lilies (Yucca spp.), so several species are grown around the world as ornamentals. Most of the ~40 known species grow as shrubs or trees with spiky, sword-shaped leaves; they produce large clusters (panicles) of bell-shaped, creamy-white flowers on stalks rising from the centre of the plant. Yuccas are symbolic of their places of origin, the great open spaces of the American and Mexican deserts. They definitely appealed to German-American physician and botanist George Engelmann (1809-1884), who became the world’s authority on the genus.
Yucca forest in San Luis Potosi, Mexico © Tomas Castelazo, Wikimedia Commons:
A cultivated Adam’s needle (Y. gloriosa) © Magnus Manske, Wikimedia Commons:
From his observations, Engelmann suspected that yucca flowers did not self-fertilize because of their morphology. Their anthers are orientated away and at a different level from the stigma, making it difficult for pollen grains to move from the former to the latter. To make the task even more challenging, yucca pollen is viscous, forming dollops not easily broken apart. Because yuccas tend to bloom at night, Engelmann reasoned that moths must be involved in pollen transport. In 1872, he collected some small, nondescript, whitish moths seen gallivanting around yucca flowers and gave them to British-American entomologist Charles Riley (1843-1895). Geographical serendipity helped Engelmann’s generous act of scientific collaboration: both men lived in St. Louis (Missouri).
Flower of a Spanish bayonet (Y. aloifolia). From The Yucca Moth and Yucca Pollination, by C.V. Riley, 1892. Wikimedia Commons.
Riley took up the challenge, and his discoveries about the role of those obscure white moths in yuccas reproduction were nothing short of spectacular; in a letter to Joseph Hooker in 1874, Darwin described Riley’s findings as ‘the most wonderful case of fertilisation ever published’.
Riley identified and named the yucca moth as Tegeticula yuccasella, from the family Prodoxidae (subsequently, several species from the genera Tegeticula and Parategeticula have been recognised as yucca moths; they are difficult to tell apart, but all more or less follow the T. yuccasella pattern). After mating on a flower of soapweed yucca (Y. glauca) or a related species, the female scrapes pollen from the anthers with a pair of specialised, spiky tentacles: these structures, which are found in no other group of insects, replace the long ‘tongue’ (proboscis) characteristic of most moths and butterflies. Without a tongue, the yucca moth can’t feed. But that’s not a problem, since the moth’s life is very short. The female uses her tentacles and sometimes forelegs to compress the glutinous mass into a ball containing up to 10,000 pollen grains, and holds it under her ‘chin’.
A female T. yuccasella carrying yucca pollen in her tentacles, which are absent in males © Jim Petranka, North Carolina Biodiversity Project:
Done with pollen gathering, the moth takes flight in search of another flowering yucca – not an easy job, as the pollen load may weigh up to 10% of her body mass. On arrival, she walks to the base of a flower to find its ovary, opens a small hole in it and lays her eggs inside. Things then become truly interesting. By using the tips of her tentacles, the moth removes a small portion of her pollen load, walks to a stigma and places the pollen on it. You can watch these steps unfolding.
Before leaving the flower, the moth marks it with a pheromone to prompt latecomers to look somewhere else for their own egg-laying. The eggs hatch and the larvae feed on some of the developing seeds. At the end of their development, the larvae leave the fruits resulting from the seeds, fall to the ground, bury themselves in the soil, build their cocoons, and start a new cycle in the following spring.
L: a female T. yuccasella gathering pollen, by C.V. Riley, 1892. R: A Tegeticula sp. moth depositing pollen on a stigma of a yucca © Sherwin Carlquist, Wikimedia Commons:
The yucca moth’s actions deserve pause for thought. When we say that an insect has pollinated a flower, we may assume it’s a deliberate act: almost invariably, that’s not the case. A pollinator would eat or take all pollen back to its nest if it could. Pollination happens by accident, when the flower visitor drops off a few pollen grains in the right spot, or has pollen brushed off by touching some part of the flower. Bees may carry away 95 to 99% of all pollen gathered, leaving the remainder – unintentionally – for pollination. But it is tit for tat in these liaisons: plants have developed adaptations to minimise pollen harvesting, such as inconspicuous anthers, narrow floral tubes, difficult flower structures, or progressive pollen release to force pollinators to make repeated visits. Some plants like orchids also cheat by attracting pollinators with scent but not giving any nectar or pollen in return. Rather than collaborating, then, insects and flowers are taking advantage of each other. Granted, this mutualistic exploitation has been fine-tuned by natural selection to avoid disastrous imbalances: overly rapacious insects and pollen-stingy plants would collapse their dealings. But unusually for these give-and-take relationships, the yucca moth deliberately pollinates yucca flowers. This process guarantees the yucca a faithful and efficient pollinator for the price of a few seeds, while the moth is compensated for its troubles with a safe and nutritious site for its offspring.
Riley, an early evolutionist, understood immediately the implications of this exchanged back-scratching. “These peculiarities are (…) mutually and reciprocally beneficial, so that the plant and the animal are each influenced and modified by the other, and the same laws which produced the beneficial specialization of parts would maintain them by the elimination of all forms tending to depart from them” (Riley, 1873. Transactions of the Academy of Science of Saint Louis 3: 55-64). Darwinian references didn’t go well with evolution-hesitant Engelmann, who mumbled that “such theories would lead us astray” – see Sheppard & Oliver (2004) for a detailed account of Riley and Engelmann’s professional relationship.
It’s not surprising, then, that Riley’s findings thrilled Darwin, who briefly mentioned reciprocally beneficial flower and pollinator traits in the Origin (1859), and developed the idea – which he called co-adaptation – in his book on orchid pollination (1862). Darwin famously predicted that a Madagascan orchid with a very long spur (a tubular projection where nectar is stored), known today as the Darwin orchid (Angraecum sesquipedale), had co-adapted with a then unknown hawkmoth with an exceptionally long tongue. And his prediction turned out to be right.
The concept of co-adaptation was renamed ‘coevolution’ by Ehrlich & Raven (1964) in their celebrated paper on butterflies and their host plants, and it is today understood as a reciprocal evolutionary change resulting from the interactions between species. The extent of coevolution as a force behind pollination has been a matter of debate, since there isn’t much one-to-one specialization involved: insects usually pollinate many flowers, and plants in general are pollinated by more than one flower visitor. Moreover, pollination is mostly a passive byproduct of a visitation for the purposes of gathering pollen, nectar, oils, or other flower resources; see for example Johnson & Anderson (2010) for a discussion. But in the case of yuccas and their moths, it would be difficult to refute coevolution; plants and insects couldn’t survive without the intricate idiosyncrasies that favour each other.
Darwin had a reason to be pleased to learn about the contrivances of some strange plants and their cryptic pollinators from the vast North American deserts. And if Captain Frémont and Smeaton Chase knew about the delicate balance between the Joshua tree and yucca moths, they may have been bestowed a more sympathetic judgement.
Yucca moths on a yucca flower. Photo by Alan Cressler, U.S. Department of Agriculture:
- A manly job
When early European colonialists arrived to the Americas, they were puzzled by a farming practice widespread among native peoples: the planting of squash (Cucurbita pepo), beans (Phaseolus vulgaris) and maize (Zea mays) simultaneously in the same field. Such a seemingly cluttered planting system happens to provide a well-balanced, nutritious combination of essential amino acids, complex carbohydrates, fatty acids, proteins and vitamin A to farmers and their families. This intercropping method, known as the Three Sisters, made a fundamental contribution to the flourishing of the Aztec, the Maya, and other American cultures. To this day, the Three Sisters are a common sight in the Central and South American countryside.
Maize, beans and squash grown together in Mexico © Paul Rogé, Wikimedia Commons:
One of the Sisters in this fortuitous arrangement, Cucurbita pepo, comprises summer squash, acorn squash, pumpkin, marrow, and courgette – the classification of these plants is complex and far from settled. Squash flowers are either male or female, and open in the morning only, never to reopen. Not only that, their pollen quickly loses its viability, especially in hot or very cold weather. So to reproduce, squash plants need quick and efficient pollen transfer from male to female flowers. Their pollen grains are heavy and sticky, so the wind will not do. This is a job for a group of solitary bees aptly named squash bees from the genera Peponapis (13 species) and Xenoglossa (seven species), which occur throughout the Americas.
The success of the Three Sisters intercropping system was possible thanks to squash bees. Among them, the Eastern cucurbit bee or hoary squash bee (Peponapis pruinosa) is the most abundant and widespread species. This bee takes pollen exclusively from cucurbits (family Cucurbitaceae), and is the only known case of a pollinator following the range expansion of crops: as cucurbits spread throughout North America, the Eastern cucurbit bee was right on their heels.
The Eastern cucurbit bee (P. pruinosa). The name of the genus Peponapis is derived from the Greek pepo (pumpkin) and Latin apis (bee) © US Geological Survey’s Native Bee Inventory and Monitoring Program.
Honey bees, bumble bees and other insects do pollinate cucurbits: in fact, they are the main pollinators of the various Cucurbita species cultivated worldwide. But these alternative pollinators are not as reliable and efficient as the Eastern cucurbit bee. Squash produce more pollen and nectar per flower than any other bee-pollinated crop, but honey bees and bumble bees will divert their attention to other plants nearby because they don’t digest squash pollen well.
Eastern cucurbit bees crack on with flower visiting at daybreak, when it’s still too cold for honey bees and other potential pollinators. Male visits are shorter than the females’ because they don’t spend any time gathering pollen: they are looking for mates. If none is available, they skedaddle to another flower, having a break now and then for a sip of nectar to keep up their energy levels. As the morning comes to an end, the flowers close and the females divert their attention to nest building on the ground. In fields planted repeatedly with squash or pumpkin, the number of nests will increase steadily to hundreds strong. For males, the afternoon is siesta time. With no females around, they huddle together in a closed flower for a long nap, coming out covered in pollen at dawn and again ready for romance.
Eastern cucurbit bees on a squash blossom © Ilona Loser, Wikimedia Commons:
Males don’t have scopa (pollen-collecting hairs) on their hind legs as females do, so they are poor pollen carriers. But they practically live on and around flowers, so the few pollen grains attached to them have a good chance of ending up on a female flower. Males are also more abundant than females, which further compensates their morphological shortcomings. It takes six to ten visits to fully pollinate a female flower: a male Eastern cucurbit bee can do that within the first hour of a flower opening. So, in all likelihood, males do most of squash pollination (Cane et al., 2011).
A male Eastern cucurbit bee on a male pumpkin flower © Elsa Youngsteadt, National Science Foundation:
The case of the Eastern cucurbit bee highlights an often overlooked aspect of pollination ecology. Traditionally, males are seen as lazy freeloaders with little to contribute to society (we are still talking about bees here). But drones, or male honey bees, produce body heat that helps maintain the temperature of the hive. And male bumble bees appear to help care for the immature forms, including by incubating pupae. Males of many bee species are poor pollinators, but that’s not the case for the Eastern cucurbit bee, and certainly for many other species yet to be investigated. Three cheers then for the unsung male bees.
A close view of a male P. pruinosa © US Geological Survey’s Native Bee Inventory and Monitoring Program.
On the U.S. of A. theme. Many years ago, I was drifting through the streets of New Orleans at the crack of dawn, as one does, when I was attracted to the sound of blues coming from the riverside. There was no other soul around besides a musician, me, and an uncurious cat: the melody cut through the crisp morning and seemed to diffuse across the city and over the river. After listening for a while, it was to find a McDonald’s. I left the man to his homage to the mighty Mississippi.
Deep South Blues:
On a return visit to the city, someone broke into my barge (a Ford Torino) and pilfered my camera & lenses. It was the end of my paparazzo career.
12 thoughts on “Readers’ wildlife photos”
The distinction between incidental pollination (where the insect happens to carry some pollen from plant to plant in the act of doing something unrelated—such as feeding) and deliberate pollination (in the case of the moths pollenating Yuccas) seems to represent a big gulf. Does that distinction—between incidental and deliberate pollination—have a name? I always thought that co-evolution or co-adaptation broadly covered both without distinguishing them. (Despite a half-career as a paleobiologist I could be wrong.) The difference between incidental and deliberate pollination reminds me of the difference between Batesian and Mullerian mimicry, where the two types of mimicry are recognized with their own names.
I know that the above is “inside baseball” and may not be of interest to everyone. 🙂
It’s hard to imagine the intermediate steps taken to get to this collaboration. The female moth lays her eggs and then pollinates the flower. She has to do that or there will be no seeds for her larvae to eat, but I’m sure she doesn’t know that! I’m not postulating an intelligent designer, but wondering if this started as an accidental pollination, that got reinforced and more profitable for each side when a quid pro quo came into play.
Great guest post! Very informative, and nice to get a personal story & evocative photo in the Appendix.
Thanks Athayde Tonhasca Júnior!
Very informative. Another interesting plant is the Schuss-Yucca documented by Gustav Albrecht.
“this plant (which Albrecht described as “a rare variety of chaparral yucca”) was that it grew ten to twenty feet straight up into the air, blossomed, and then died, all within “a manner of minutes or even seconds.””
The Scientific Monthly
Vol. 75, No. 4 (Oct., 1952), pp. 250-252 (3 pages)
Published By: American Association for the Advancement of Science
Absolutely riveting, as always. So sorry about your camera!
Such an interesting post! Many thanks.
Interesting that Fremont mentions Poe. Fremont was, of course, the 1856 Republican Presidential nominee: “Free Soil, Free Labor, Free Speech, Free Men, and Fremont!”
Thanks Athayde for another riveting and educational post. I wonder what the band U2 thinks of the Joshua tree…maybe they were more interested in the biblical reference (though Mormons named the tree!). I’ve seen the tree in person, and thought it beautifully armored.
Sorry about the break-in, happens to the best of us. I’ve had a couple car stereos and numerous CDs snatched, but thankfully never a beloved camera with multiple lenses. Yikes!
Thanks, everyone. Being camera-less had a positive side: a lighter, more agile way to explore.
An excellent post – these are always a treat. Very many thanks!
Traditionally, males are seen as lazy freeloaders with little to contribute to society (we are still talking about bees here). LOL!
I love your posts for their variety and technical detail, always a delight to read and keep.
Thank you very much.
Those who wish to learn much more about Joshua Trees should go here: