Come in – if you insist

By Athayde Tonhasca

Philip Miller (1691-1771), author of the renowned The Gardeners Dictionary and Fellow of the Royal Society, was a keen experimenter in plant propagation. In a 1715 letter to a friend, Miller described his observations of bees visiting tulip flowers, “which persuades him that the Farina may be carried from Place to Place by Insects” – Farina is the Farina Fecundens (fertilizing flour), or pollen, which fellow naturalists suspected played an important part in plant reproduction. Meanwhile in America, Arthur Dobbs (1689-1765), Governor of North Carolina, promoter of expeditions in search of the Northwest Passage and amateur scientist, came to a similar conclusion: “I think that Providence has appointed the Bee to be very instrumental in promoting the Increase of Vegetables”.

His excellency Arthur Dobbs esq., captain general, governor in chief and vice admiral of the Province of North Carolina in America, circa 1753 © The New York Public Library Digital Collections.

Philip Miller and Arthur Dobbs were two of the pioneer naturalists who recognised and assessed the role of insects in plant reproduction. We learned a great deal since then, so that today plant-pollinator associations are considered some of the best examples of mutualisms, that is, relationships between two species that benefit both. ‘Mutualism’ invokes noble concepts such as cooperation, teamwork, union, and common good; so, analogies with human behaviour were just too tempting. The anarchist Peter Kropotkin (1842-1921) cited examples of mutualism in the natural world as arguments against ruthless competition in human societies, while ecologist Warder Clyde Allee (1885-1955) and colleagues, in their influential Principles of Animal Ecology, made numerous references to human cooperation in discussions about mutualism (Boucher et al., 1982). These comparisons with human values risk distorting the true character of mutualism in the natural world, as is the case with pollination. There’s little collaboration here: plants give away as little pollen and nectar as possible because these products are metabolically expensive; sometimes they cheat, giving no reward at all to flower visitors. Pollinators on the other hand would take as much resource as possible, with no altruistic regard for plants’ needs. Instead of cooperation, this type of relationship is best described as mutual exploitation (Westerkamp, 1996). Or, as Danforth et al. (2019) put it, ‘pollinators are like an overly demanding lover – they are great to have around at times, but if left without boundaries, they can take over your life and ruin it.’

Plants are in a delicate position: they need to attract insects to transfer their pollen but must be parsimonious in their rewards, otherwise these will be quickly depleted. To sort out this dilemma, many species evolved a range of adaptations to regulate access to pollen and nectar, and to discourage floral robbers (consumers that do not pollinate). Some plants exclude unsuitable visitors by restricting their pollen to specialised buzz pollinators; others rely on explosive pollen release, while some take the route of morphological tinkering such as keel flowers.

Keel flowers have five petals: a large one on top called the banner (also known as the vexillum or standard petal), two concave ones on the sides (the lateral wings or alae), and two at the base: these are stuck together to form the keel, which encloses the reproductive organs.

Parts of a keel flower: 1. Banner; 2. Wings; 3. Keel © Kembangraps, Wikimedia Commons.

Keel flowers are common in the subfamily Papilionoideae (or Faboideae) of the legume family (Fabaceae). They are also known as papilionate flowers, from their resemblance to butterflies – papilio in Latin. Papilionoideae comprises an estimated 14,000 species, or over 70% of all legumes. They are found in a range of habitats, and many of them are important sources of human and animal food, such as soybean (Glycine max), beans (Phaseolus spp.), clovers (Trifoliumspp.) alfalfa (Medicago sativa) and peanut (Arachis hypogaea).

The ungainly shapes of keel flowers seem to have been designed to make life a bit difficult for pollinators. Not to put them off completely – that would be suicidal – but to make them work hard for their reward. To access the nectar, a visitor must grab the flower, push the keel down, while simultaneously prising apart the lateral wings, engaging their legs and mouth in elaborate contortions. These manoeuvres expose the stigma (female parts) and the anthers (male parts), which touch the visitor and ensure pollen transfer. 

Brown hemp (Crotalaria juncea) pollination. a: Megachile bicolor grabbing the base of the banner with its mandibles; b, c: M. bicolor and M. lanata pushing against the lateral wings with their legs and abdomen, so that style and anthers touch the bees’ scopa (pollen gathering bristles); d: the carpenter bee Xylocopa fenestrata repeating the process © Kumar et al., 2019.

These operations require strength and technique; visitors that do not have the physical apparatus or sufficient power such as butterflies and flies are mostly excluded from keel flowers. Hummingbirds and other birds are also barred, as they can’t open the petals with their beaks and the keels are not big enough for landing (Westerkamp, 1997). Only bees, and only the larger ones at that, can deal with the challenge. Watch bumble bees expertly working their way around lupin (Lupinus sp.) flowers, and note the spike-like structure – the keel – poking out between the lateral wings as bees push them apart. On touching the keel, bees are dusted with pollen. And here, a leafcutter bee (family Megachilidae) illustrates the labour required to get the nectar in a brown hemp flower.

Keel flowers block the less desirable visitors, saving pollen and nectar for the reliable larger bees. It’s not surprising then that so many plant species have adopted this aesthetically peculiar but highly effective flower shape.

See no weevil, hear no weevil

By Athayde Tonhasca

As the story goes, J.B.S. Haldane (1892-1964), British/Indian geneticist, evolutionary biologist and mathematician, found himself in the company of a group of theologians. On being asked what one could learn about The Creator from studying his creation, the atheist Haldane is said to have answered ‘an inordinate fondness for beetles.’ Haldane may have said something like that, and indeed a Great Architect of the Universe would have had to be partial to the order Coleoptera. With nearly 400,000 known species, beetles lead the biodiversity table, making up about 25% of all known animal species. But if the Almighty Creator liked beetles, he was especially fond of weevils (superfamily Curculionoidea): there are over 97,000 described species, of which 76,761 are snout beetles (family Curculionidae) (Global Biodiversity Information Facility). But we know these figures are gross underestimations because in poorly studied areas, i.e., most of the world, the majority of weevil specimens collected are from unknown species.

A circular tree of life for some described eukaryote groups (all organisms except bacteria and bacteria-like Archaea). Insects – in the left column – make up about 63% of the total. Vertebrates, together with other deuterostomes (animals for which the anus is formed before the mouth during embryonic development) are a mere ‘etcetera’ in the big scheme of life. Their biodiversity is comparable to weevils’ © Adam Dent, Wikimedia Commons.

Weevils are found practically everywhere, and almost all of them are plant eaters. They feed on plants from any terrestrial or freshwater habitats and on a range of tissues: roots, stems, phloem, fruits, flowers or seeds. Many species are among the most damaging pests of stored grain, field crops, orchards, ornamental plants and commercial forests. Weevils’ destructive potential can’t be overestimated. The boll weevil (Anthonomus grandis) wrecked the American cotton industry in the 1920s and 30s, then invaded South America in the 80s for further mayhem. In the US, the Southern pine beetle (Dendroctonus frontalis) is able to wipe out thousands of hectares of pine in less than two years, while grain weevils (Sitophilus spp.) can completely destroy rice, maize, wheat, oats, and many other products stored is silos around the world. You may have had your own experience with weevils infesting a bag of flour or a box of pasta in your pantry.

Rice weevils (S. oryzae), a pest of stored grains and cereal products. Some weevils don’t have the long snout characteristic of the group, and not all long-snouted beetles are weevils © CSIRO, Wikimedia Commons.

Considering weevils’ charge sheet, we would be tempted to dump the lot in the ‘creepy crawlers’ category. But that would be hasty and unjustified. Only a tiny minority of weevils are harmful, while the great majority contribute to the functioning of ecosystems. One way they do this is by pollinating a range of plants.

Cantharophily (from the Greek word kántharos for beetle), or pollination by beetles, is not well understood or researched, despite being one of the first pollinating systems in the evolutionary history of flowering plants. With time, bees, flies and moths became the main pollinators, but many plants, especially of ancient lineages such as magnolias (Magnoliaceae), retained cantharophily. Some custard apple-related plants (Annonaceae), arums (Araceae), palms (Arecaceae) and orchids (Orchidaceae) are also pollinated by beetles.

Most beetles don’t handle pollination skilfully and gently: they plough through flowers, gobbling down nectar, pollen or petals, defecating as they go, often spilling more pollen than they eat – that’s why they are called ‘mess and soil’ pollinators. During these raids, beetles become contaminated with pollen grains, which are deposited on the next plant they visit. Weevils, however, have a more intimate and nuanced rapport with their hosts. They lay their eggs on the flowers, where their larvae will grow and mature by feeding on pollen, ovules, or other floral parts. By hosting weevils during a significant portion of their lives, plants are almost guaranteed being pollinated for the price of a fraction of their reproductive parts. 

This type of mutualistic relationship is known as brood-site pollination or nursery pollination and it has been reported dozens of times for different groups of insects, mostly in the tropics; the interactions between figs and wasps and between yuccas and moths are two of the better known examples. In the case of weevils, hundreds of species have coevolved brood-site associations with a range of plants, but mostly with palms (family Arecaceae). 

Pupa (A), egg (B) and larvae (C-F) of weevils growing in different inflorescence parts of palms. Credits: A, F: J. Haran, B-E: B. de Medeiros © Haran et al., 2023.

One instance of weevil-palm mutualism has particular relevance for its ecological and economic implications: the pollination of African oil palm (Elaeis guineensis) by the African oil palm weevil (Elaeidobius kamerunicus). Male weevils feed on the palm’s flowers and pollen, while females oviposit in the flower structures, in which the larvae feed and develop. You can watch the weevils in action.

When oil palm growers around the world, but mostly in Indonesia and Malaysia (the leading producers and exporters of palm oil), began to import the pollinating weevil in 1981, the industry changed radically. The beetle adapted well to its new habitats and boosted African oil palm pollination, which resulted in sharp increases in production, revenue and applications; palm oil made its way into margarines, chocolates, baked products, cooking oils, soap, detergents, cosmetics – you name it. The “million dollar weevil” had been found (Robins, 2021). 

A female African oil palm weevil, and weevils clustering on palm flowers © Ken Walker, Museum Victoria, CABI (L) and Susenoqurnia, Wikimedia Commons.

But as sociologist Robert K. Merton warned us, purposeful actions are bound to have multiple outcomes, some of them unanticipated. This law of unintended consequences (flippantly identified as Murphy’s Law) suited the case of the million dollar weevil to a T. Large-scale oil palm production resulted in massive deforestation that is destroying the habitats of large numbers of plant and animal species, and increased levels of erosion and pollution.

Fortunately, the introduced African oil palm weevil is an isolated case of ecological mishap. All other known examples of beetle brood-site pollination are mutualisms that help maintain biodiversity. Seres & Ramirez (1995) estimated that more than 45% of palms and herbs in some cloud forests are beetle‐pollinated, and Haran et al. (2023) have recorded at least 600 cases or suspected cases of palm-weevil interactions: the true number is likely to be much larger. We have the vaguest understanding of the pollinating services played by these weevils, but it mustn’t be something to sniff at considering that the number of Curculionidae species alone is almost four times bigger than the number of bee species (~20,000). 

Palms and many other types of plant pollinated by weevils are sources of food, building materials, cosmetics and medicines; a good portion of those products are consumed locally or sold abroad, generating much needed income to developing countries. Not so bad for those maligned big-conked characters.   

According to biblical sources, Noah’s ark had ~42,500 m³ of available space, the equivalent of 570 standard railroad stock cars. We can deduce that Noah’s ship was not a run-of-the-mill zoo because most species competing for a berth comprised parasites and weevils. Art by Simon de Myle, 1570. Wikimedia Commons.