The times they are a-changin’.

By Athayde Tonhasca

In winter I get up at night

And dress by yellow candle-light.

In summer, quite the other way,

I have to go to bed by day.

Bed in Summer, Robert Louis Stevenson

R.L. Stevenson’s light-hearted rant may have been inspired by a youth’s frustration with the vicissitudes of the seasons, but these variations are vital for life on Earth. Many biological events such as migration, egg laying, spawning, flowering and hibernation follow cyclical or seasonal timing: the reproduction and survival of countless organisms depend on this natural calendar. These periodic biological phenomena and the branch of science dealing with them are known as phenology. 

Season-wide flowering curves for a montane plant community in Colorado, USA © CaraDonna et al., 2014. PNAS 111: 4916-4921.

For some species, life cycle events are triggered by the onset of rainfall, or by a day-length threshold (photoperiod); genetics also plays a role. But the great seasonal regulator is temperature, which affects so much of organisms’ activity and metabolism. It is no surprise, then, that phenology is considered to be one of the best tools to assess the effects of climate change.

Many spring and summer phenological events have advanced in the calendar for many groups of organisms, and these changes have been consistent with increasing average temperatures. Among these effects, the onset of blooming is well documented; several plants seem to be responding to a warmer world during the last 20–50 years by flowering earlier. In Britain, flowering has advanced by almost one month since 1986, and many species are flowering nearly one week earlier in the south and in lower elevations when compared to northern areas and higher elevations, respectively. These changes have been relentless: between 1952 and 2019, the British flora has experienced an average advancement of 5.4 days every ten years.

First flowering dates between 1753 and 2019 and their distribution for older (1753–1986) and recent (1987–2019) dates. There is a difference of 26 days between older and recent © Büntgen et al., 2022. Proc. R. Soc. B 2892021245620212456

These variations can have many consequences because plant phenology influences the abundance and distribution of organisms, ecosystem services, food webs, and cycles of water and carbon. Even people can be directly affected by these deviations, as for example by the timing of planting, fertilizing, and harvesting crops, and the production of allergy-triggering pollen.

Of course insects could not be immune to climate change. In the Northern Hemisphere, warming has caused species distributions to shift northwards or upwards in mountainous areas. Indeed, the abundance of many butterflies, beetles, dragonflies and grasshoppers have contracted at low latitudes and elevations, and increased in northern areas and at higher altitudes. Some bumble bees do not appear to track the weather, but their spring flight times have advanced.

Plants and pollinators are undergoing rapid variations in their phenological patterns. But if these changes happen at different rates or magnitudes, pollination may become out of sync, with temporal or spatial mismatches. For flowers, there could be reduced visitation rates and pollen deposition; for pollinators, there could be less nectar and pollen.

Plant-pollinator asynchronies may cause concern, but there are few studies assessing their effects. This is not surprising because long-term field observations are afflicted by ‘noise’ such as unusual weather spells, pollinators’ travels from one site to another, and difficulties in recording the onset of phenological events. Long-term data are needed. This requires a clipboard, a pencil, compliant subjects, and a great reserve of patience.

The orange-legged furrow bee (Halictus rubicundus) was just the ticket. This bee is widely distributed throughout Britain and the Northern Hemisphere. It builds its nest in the ground, often in large aggregations, and in a variety of habitats. It visits many flowers, especially composites such as ragwort, thistle, and knapweed.

A female orange-legged furrow bee © linsepatron, Wikipedia Creative Commons

A population of orange-legged furrow bees in the American state of Utah was monitored daily for 22 years for the detection of the first day of nesting and its possible relation with the bee’s environment. It turned out that time of nesting varied widely (a range of 44 days), but was much more determined by temperature than calendar date. 

Cumulative degree days (the amount of time that the insect spends at temperatures within its development range) for the actual (black) and median (red) dates of orange-legged furrow bee emergence © Cane, 2021. Insects 12: 457

Most importantly, bees’ activity and blooming in the surrounding area remained roughly synchronised: bees and plants seem to respond to the same environmental cues. Similar results were obtained from long-term observations (12 to 14 years) for the Eastern cucurbit bee (Peponapis pruinosa), the South-eastern blueberry bee (Habropoda laboriosa) and the tawny mining bee (Andrena fulva), a common British species that seems to be spreading rapidly into Scotland.

A female tawny mining bee © gailhampshire, Wikipedia Creative Commons

Other studies have suggested that plant-pollinator interactions are resilient to climate change: flowers and their pollinators seem to be keeping pace with each other. Even more puzzling, the seasonal timings of some species have become closer instead of further apart. This apparent tolerance for a rapidly changing environment is helped by the flexibility of pollination interactions: most pollinators visit multiple plant species, and most plant species are visited by many pollinators; one to one relationships are rare.

Plant-pollinator mismatching doesn’t seem to be occurring to a significant degree, which is a rare case of climate-related good news. But like anything else in nature, there are limits. If temperatures and the frequency of extreme weather events do not relent, the fine-tuned relationships between plants and their insect pollinators may start to unravel. And that would mean trouble for all of us.

It was all yellow

Near where I live occurs an annual delight.  It’s the February carpet of glossy winter aconites that dazzle on an otherwise unremarkable muddy bank.  They jostle for attention with a smattering of bright snowdrops, but it’s the yellow Eranthis hyemalis that catch my eye. There is something deeply cheerful about a bright yellow flower at this time of year. 

The winter aconite is one of the few plants in flower at the moment and is reckoned to be a native of south west continental Europe, and, just like the snowdrop, is naturalised in the UK.  It has nothing to do with the ‘real’ aconite.  Instead, it’s a member of the buttercup family that thrives in deep deciduous woodland where it flowers before the tree canopy opens.

Without leaves ‘getting in the way’, light gets to ground level even at this time of year, encouraging the flowers to open up and become more easily visible.  The novelist D.H. Lawrence called the winter aconite one of the most charming flowers.

There are around 20 species of bumblebee to identify in Scotland, a mere fraction of the floral catalogue surely.  Gradually my botanical ID skills are improving, but they still aren’t that good. Yellow flowers are a particular challenge – so many, so many.   I doubt I’ll ever be fully confident about what I’ve seen, and suspect that reference books will always have to be consulted. From dandelion to coltsfoot, from ragwort to hawkbit, buttercup to marsh marigold, I find it a challenge. And until recently winter aconite and lesser celandine had me scratching my head.

Winter aconite often flowers amongst leaf litter.

As an early source of nectar and pollen, winter aconite certainly plays a role in helping insects that venture out before spring is fully in swing. I’ve found this yellow carpet to be a good spot for early pollinator sightings.  Mainly flies, but the odd bee from time to time. 

The petals are not what they seem!  Our classical flowers have a ring of petals, and sitting just beneath them a ring of sepals.  The petals are usually coloured and the sepals are usually green, like tiny green petals.  In some flowers the petals and sepals are the same colour and together are known as “tepals”.  In winter aconite the flower has yellow sepals.  

There is scope for confusion with other aspects of winter aconite. Eranthis hyemalis is a challenging name. On the one hand the Latin hyemalis suggests ‘wintry’ or “winter-flowering” – but in Greek the name Eranthis can be broken down into Er giving an association with ‘Spring’, and Anthos which points to ‘flower’. Either way it’s an early delight for botanists.

Bex Outram, who was once a colleague of mine at NatureScot, captured the essence of winter aconite’s appeal in a piece on the National Trust for Scotand website thus … “The small yellow flowers pop their heads out very early in the year, which seems like an unusual tactic for a flowering plant. However, as with everything in nature, there’s method in the madness! It grows most abundantly in deciduous woodlands, and the strategy of flowering early enables it to take advantage of the maximum amount of sunlight penetrating the canopy without the leaves blocking the light. Being one of the earliest flowering plants, it has very little else to compete with for light and nutrients at this time of year.”

Bex was spot on.  A low-to-the-ground plant, winter aconite creates a stunning display of yellow in what can be a grey time of year.  It certainly lifts the spirits of many, and for any passing pollinator it’s especially welcome on a winter’s day.

Find out more about winter aconite

Summary and distribution in the UK

Blanket of gold : The New York Met Museum article on winter aconites

The night of the living dead

By Athayde Tonhasca

A cold, drizzly night falls on an apiary somewhere in America. All seems quiet, until one of the resident honey bees (Apis mellifera) does something odd: she emerges from the hive and flies towards a streetlight glowing faintly in the distance. A few of her sisters take off as well, but some of them fall to the ground and walk around in circles, apparently confused. None of these night wanderers will ever return to the hive; soon they will all be dead. They have been victims of a parasite ominously named the zombie fly (Apocephalus borealis).

A female zombie fly © Core et al., 2012. PLoS One 7(1): e29639

This fly belongs to one of the largest insect groups, the family Phoridae. They comprise about 4,000 described species, but specialists believe this number represents about 10% of the total. Phorids look like fruit flies with arched backs, and when spooked they run away before taking flight. Such behaviours explain their common names: hump-backed flies or scuttle flies. They are found everywhere, and include species with a variety of feeding habits such as saprophages (they eat decaying organic matter), predators, and plant feeders. One species is a serious pest of cultivated mushrooms. 

Two groups of Phorid flies, the genera Pseudacteon and Apocephalus, are found mostly in South America and are charmingly known as ant-decapitating flies. These are parasitoids (insects that are free living as adults and parasitic as larvae, eventually killing their hosts). An ant-decapitating fly approaches its target from behind and uses its powerful, hooked ovipositor to inject an egg in the victim’s head or thorax.

The hooked ovipositor of Pseudacteon curvatus, a fire ant-decapitating fly © Sanford Porter, Wikipedia Creative Commons

The resulting larva moves to the ant’s head, where it feeds on hemolymph (‘blood’) and tissues. Eventually, the larva consumes all the head contends, causing the ant to wander around with no purpose. In two to four weeks, the larva is ready to pupate. It releases enzymes that dissolve the tissues attaching the ant’s head to its body. The head falls off, and the fly pupates inside it before emerging as an adult. These flies are bad news for ants, and therefore are promising as biological control agents against invasive species such as fire-ants (Solenopsis spp.). 

A) An ant-decapitating fly (Pseudacteon sp.) preparing to inject an egg into the thorax of a fire ant. B) A decapitated ant with a fly maggot consuming the contents of its head © Porter & Gilbert, 2005. International Symposium on Biological Control of Arthropods

The zombie fly does not decapitate honey bees, but much of its life history is similar to those of its tropical relatives. It lays its eggs in the abdomen of the bee. The larvae feed on hemolymph and flight muscles, and when they are done, they leave the host to pupate outside. Up to 13 larvae have been observed coming out of a dead honey bee.

A zombie fly ovipositing into the abdomen of a honey bee worker, and two fly larvae leaving the host at the junction of the head and thorax © Core et al., 2012. PLoS One 7(1): e29639

We don’t know why a parasitized honey bee would abandon her nest, especially at night, to wander on a suicidal excursion. Her neurological wiring may have been highjacked by the fly; many parasites and parasitoids such as thick-headed flies alter their hosts’ behaviour for their own benefit. The zombie fly may have induced the bee to seek a safer place for the development of her eggs and larvae. Alternatively, the infected bee may have been forced out by her healthy sisters. Or the doomed bee left on her own, acting on a well-adapted altruistic instinct to avoid an epidemic.

Four zombie fly pupae surrounding the dead honey bee from which they emerged © John Hafernik, University of Florida Entomology and Nematology Department

The zombie fly is native to North America, where it has long been known to parasitize bumble bees and wasps. Then in 2009, there was an alarming discovery: the fly was also attacking honey bees in parts of the United States. And there was more bad news to come. The zombie fly was shown to harbour the fungus Nosema ceranae and the deformed wing virus, which are serious problems to honey bees. Researchers don’t know yet whether the zombie fly plays a role in the transmission of those pathogens to bees, but the possibility is ominous.

We may look at the plight of American honey bees with the detachment reserved for someone else’s problem, but that would be unwise. In 2013, zombie fly genetic material (ribosomal RNA) was found in honey bees from Belgium. In other words, this parasitoid may be in Europe already, lurking undetected. If so, it could easily hop across the English Channel. British beekeepers have a handful of pest and diseases to deal with already – the zombie fly would be another headache of unknown magnitude. The honey bee is the single most important crop pollinator worldwide, so the spread of a novel parasite could be serious, if not disastrous. 

The possibility of a zombie fly invasion is a reminder of the hazards posed by alien species. With the ever-increasing traffic of people and goods around the world, and a climate more accommodating thanks to global warming, we may hear more and more about these uninvited, unpleasant and unwelcome guests that may threaten our pollination services. 

The number of border insect interceptions (log scale) in Europe © Bacon et al., 2012. PLoS ONE 7(10): e47689.

Small is ok

By Athayde Tonhasca

Gardeners, land managers, conservation groups and local authorities have been planting away to provide food for pollinators. Such commendable efforts have resulted in great swathes of flowering plants, often in the form of road verges, uncultivated crop margins, or un-mowed land strips. These large floral areas are beneficial and quite convenient for a range of pollinators, who can hop effortlessly from flower to flower to gather pollen and nectar. High plant density reduces foraging costs – in the form of energy expenditure – and increases visitation rates. Bumble bees for example are known to take advantage of high flower concentration.

A wildflower meadow: a profusion of pollinators’ food © Richard Croft, Wikipedia Creative Commons

But high flower abundance may have negative consequences. Visiting insects may not keep up with the task, so some flowers may receive an insufficient number of pollen grains – or none at all. Flower-rich areas attract lots of pollinators, who may compete with each other for resources: smaller, slower species may have hard times finding flowers not already cleaned out by more efficient visitors.

Smaller flower patches don’t attract many pollinators because the limited food supply may not be worth the effort of flying to them. But those that take their chances may be compensated by less competition and greater energy efficiency, as they are less likely to come across flowers depleted of nectar and pollen by a previous visitor. Being in a small group can be good for plants too: each one of them has a better chance of being visited.

So there are opposing effects at play. Larger flower patches attract more visitors, but pollinators may face hard competition, and the visitation of individual flowers may be compromised. Smaller patches can be costly to visit, but flowers may be more rewarding individually.

A variety of observations and studies at different locations and settings have demonstrated that in the case of bees, the balance tilts in favour of bigger:  the higher the floral abundance, the greater bee diversity and numbers. But not all bees follow this pattern: some small carpenter bees (Ceratina spp.) and halictid bees (family Halictidae), especially base-banded furrow bees (Lasioglossum spp.) seem to prefer isolated clumps of flowering plants over large swathes of habitat. This choice has been, at least partially, attributed to the need for escaping competition with the ever-present bumble bees.

A blue carpenter bee (Ceratina cyanea) (L) and a common furrow-bee (Lasioglossum calceatum) © Hectonichus (L) and Martin Cooper, Wikipedia Creative Commons

Only one species of small carpenter bee occurs in Britain, but there are around 34 species of base-banded furrow bees; the exact number is uncertain because they are difficult to identify and monitor. These bees visit a wide range of flowers, although their role as pollinators is not well understood. Elsewhere, they have been shown to pollinate melons and tomatoes, among other plants.

Extensive pollinator habitats are not always viable because space or resources are limited, as for example in urban settings. But smaller areas play their part by catering for the set of crowd-shy pollinators, which is likely to include species other than small carpenter and halictid bees: we have information about foraging habits of only a fraction of pollinating species. 

A small island of pollinators’ habitat in a private yard in Oakland, USA © Akos Kokai, Wikipedia Creative Commons

It also helps to keep in mind that most pollinators are highly mobile. For a bee in search of pollen or nectar, a small garden may not provide all it needs, but that islet of flowers may be a stopover on a journey over an archipelago of food sources. Small bees normally forage within 100 to 300 m from their nests (the bigger the bee, the further it goes), but if pressed by hunger, they can fly over 1 km to collect pollen or nectar. Larger species like bumble bees and honey bees make much longer foraging trips.

So if you ever question whether a flower box, a strip of flowers along a fence, or a tiny flower bed in a parking lot make any difference, the answer is yes.

A kitchen garden with a segment set aside for flowers © Ukiws, Wikipedia Creative Commons

Riverside’s Stirling success

Our guest blog today comes from Stirling’s ‘Riverside Naturally’, a community group that works to develop open spaces in environmentally friendly ways.  They’re based in the area covered by Riverside Community Council in Stirling, which includes both Riverside, a residential area, and Forthside, a commercial area. It is bounded by the river Forth and the mainline railway line.  They often work in partnership with Stirling Council.

By Pat Morrissey

I suppose it’s almost a truism that no tree dies without giving: nutrients are returned to the soil, invertebrates benefit from the breakdown of tissue, and a whole new biodiverse environment can be created if the wood isn’t carted away, shredded or burned. But what if the death of a tree gave birth to local environmental ecological activism that resulted in many more trees being planted, orchards being developed and maintained, wildflower meadows, woodland gardens and other areas being managed for the benefit wildlife and thereby the benefit of people? Wouldn’t that be wonderful offspring?

This is exactly what happened in Riverside in Stirling in 2019. A beautiful mature red oak was taken down much to the displeasure of local residents and, prompted by discussions around the Scottish Wildlife Trust publication “Living Cities”, a group was formed to enhance the locality to make it a better place for people, by making it a better place for nature: Riverside Naturally was born. 

In the two- and a-bit years of its existence RN has, in consultation with local partners, redesigned and replanted raised beds in the area with plants specially chosen for their appeal to pollinators. A range of annuals and perennials were grown to give a season-long source of food and shelter. Six different species of bees, innumerable hoverflies, many butterflies (and a few wasps) have been spotted feeding, resting and mating in these newly created spaces. The raised beds have been replicated in the local primary school which has resulted in opportunities to engage with staff and pupils ensuring that the children are aware of the need to support pollinators and how to provide it.

We also maintain the local community orchard which provides food for pollinators and for the local community: we have over twenty fruit trees in this site. Volunteers help maintain the orchard – weeding, pruning and composting the cuttings and grass. The trees derive a reciprocal benefit from the bees and other insects and all of our trustees, members and volunteers reap the rewards of working closely with nature and learning about the cycle of giving and receiving in the environment. In the years prior to the Covid pandemic we have held Orchard Days where members of the public are invited to share the fruits of our labours and learn of the vital roles played by plants and animals in maintaining a healthy planet. 

The charity has also converted two neglected formal garden areas in Riverside Park, removing sick and unproductive plants, and replacing them with native species of trees, shrubs and ground cover to create woodland gardens which, especially in the Springtime, will give early sources of nectar to those bugs which are active at that time of year. As this work progresses more planting will help sustain these vital insects through the year.

We also have worked in partnership with Stirling Council to designate an area around the river bank as an Area of Restorative Kindness (ARK) where the land has been planted with native species, and then only lightly maintained to allow nature to thrive at its own pace. However, to give it the best start possible we have planted seven oaks and a rowan with additional native plants scheduled for introduction in the coming months.

We have taken a strict “No Spray” stance on all of our projects as we are fully aware of the damage that can be caused to pollinators by insecticides and other harmful chemicals when used indiscriminately. Through all our projects we provide a safe haven for wildlife in general and aim to encouraging pollinators in particular. To this end we have recently built bug hotels, created wood piles and managed grass cutting to ensure that as many insects and invertebrates as possible have a place to shelter over the winter and nest in the summer.

With a growing number of volunteers and members, and overwhelmingly positive support from the local community, Riverside Naturally has offered residents and passers-by the opportunity to learn from and about nature, to have their physical and mental health improved, to celebrate and participate in the web of interconnectedness that binds us all together and helps us work towards restoring planetary wellbeing.

And … in the winter of 2019/2020 under the auspices of Riverside Community Council and Riverside Naturally, a new red oak was planted in Riverside Park which will stand testament to the hard work, optimism and long-term thinking which is at the heart of all our actions.

Website: Riverside Naturally

A manly job 

By Athayde Tonhasca

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 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, Wikipedia Creative 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 are 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. 

Male (L) and female squash flowers © Abrahami, Wikipedia Creative Commons

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 the Americas, the Eastern cucurbit bee was right on their heels.

The Eastern cucurbit bee (Peponapis 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. They will divert their attention to other flowering plants nearby, and are not completely attuned to squash, which produces more pollen and nectar per flower than any other bee-pollinated crop. But despite the abundance of pollen, honey bees and bumble bees largely avoid it because they don’t digest it well. They visit squash flowers for the promise of copious volumes of nectar.

Female Eastern cucurbit bees crack on with flower visiting at daybreak, when it’s still too cold for honey bees and other potential pollinators. Nest building is reserved for the afternoon, when flowers are closed. In fields planted repeatedly with squash or pumpkin, the number of nests will increase steadily to hundreds strong. 

Eastern cucurbit bees on a squash blossom. Ilona Loser, Wikipedia Creative Commons

There is another reason for the efficacy of these pollinators: an energetic male work force.

Female bees build their nests all over the landscape, and it would be time-consuming and costly for a male to patrol a large nesting area in search of a female. Instead, males spend their mornings frantically flying from flower to flower hoping to find a mate, taking a sip of nectar now and then to keep their energy levels. As the morning comes to a close and females become scarce, males huddle together in a closed flower for a long nap, coming out covered in pollen at dawn and again ready for romance. 

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 it seems that males do most of the visits to squash flowers.

A male Eastern cucurbit bee on a male pumpkin flower © Elsa Youngsteadt, National Science Foundation 

So what does this tale from across the Atlantic have to do with us?

It is a reminder of the relevance of pollinator specialists. While most plants and flower visitors are flexible and adaptable – squash included – sometimes the highest levels of plant reproduction and pollinator nutrition are achieved only with the right partners. Honey bees for example have replaced or complemented crop pollination services around the world, but they often fall short. 

The case of the Eastern cucurbit bee also highlights an often overlooked aspect of pollination ecology. Traditionally, males are seen as lazy free-loaders 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 likely for many other species yet to be investigated. Three cheers then for the unsung male bees.