Monitoring matters

Thanks to a range of excellent presenters, our Third Annual Pollinator Conference seemed to hit the mark in mid-June. The subject was monitoring, and our speakers were on top form. From a range of talks we got a real sense of the ‘why?’ and ‘how?’ behind monitoring our insect populations. 

The aim of the conference was to demystify recording insect numbers and trends, whilst emphasising the value of monitoring in understanding and sharing information around changes in biodiversity. Our speakers revealed how they gather information and what they do with it.

Anthony McCluskey of Butterfly Conservation opened the day by talking about insect declines and the fact that it was repeat monitoring that allowed him to make such statements with confidence. Anthony gave a good example of the value of monitoring in noting general trends and picking up on individual anomalies. In the latter category he cited the example of the orange-tip butterfly, which surveys reveal to have doubled in the past 10 years.

“Monitoring allows us to ‘take nature’s pulse’,” noted Anthony. It throws a spotlight on climate change impacts, and only with monitoring can his organisation know which species they should be concerned about.

“What makes a good monitoring record?” was a question that Anthony was keen to answer. He explained that a useful record requires a date, an approximate location, and a species identification. He gave us an insight into the iRecord butterflies app, the UK Butterfly Monitoring Scheme, and the forthcoming Garden Butterfly Survey. 

Anthony was followed by Richard Comont, Science Manager at the Bumblebee Conservation Trust and well-versed in all things bumblebees. His talk on BeeWalks was an insight into monitoring across the board. His starting point was the assertion that any conservation organisation needs accurate up to date information to know where ‘their’ species are and how they are faring. He used the Great Yellow Bumblebee as an example for where monitoring paints a valuable picture.

He then gave us an insight into BeeWalk, which is one of a suite of biological recording projects in the UK. Richard outlined how volunteers count and identify bees as they go along a set route. Richard acknowledged that some bumblebees are hard to identify, but noted that BeeWalk has an impressive record of training people in identification skills. Beewalk has fired the public imagination across the UK, with over 250,000 records submitted.

Richard gave us a lovely Scottish example of public participation in the Cairngorms, where the face-to-face Skills for Bees project is drawing increasing input from a small army of volunteers. And he concluded that good data is a cornerstone of making progress in the quest to help bumblebees thrive.

Claire Carvell, ecologist at the UK Centre for Ecology & Hydrology, gave us an insight into the increasingly popular PoMS FIT Count work. Claire explained how UK PoMS is the world’s first monitoring scheme generating systematic data on the abundance of bees, hoverflies and other flower-visiting insects at a national scale. She pointed out that UK PoMS provides much-needed evidence to the UK’s four national pollinator strategies.

She described how the Flower-Insect Timed (FIT) Count survey works, pointing out that the aim is to collect data on abundance of flower visitors and plant-pollinator interactions across a variety of habitats. Participants are advised to count all insects that land on flowers of a target flower species within a 50×50cm patch during a 10-minute period, and identify insects from broad groups.

Claire’s attractive and informative diagrams and infographics showed us how FIT Counts are revealing the importance of different insect groups to different flower types , as she explained how this data is used and communicated.

After our break, Claire’s colleague Martin Harvey, who was representing UKCEH Biological Records Centre, PoMS, and the Dipterists Forum, lifted the lid on the world of recording and monitoring flies. Given that hoverflies alone visit at least 72% of our global food crops, it was clear that Martin’s subject was important. His talk was good on details, both large and small.

For the non-dipterists in the audience, Martin included a useful ‘Fly Features’ introduction, before giving us an insight into the resources available through the Dipterists Forum. We were also taken through the crucial ‘data crunching’ that follows monitoring exercises. It was a revealing journey noting challenges and methods, and ended with Martin having made his point on just how important flies are as pollinators. 

‘Trends and the importance of monitoring’ was the title for Simon Foster’s talk.  NatureScot’s Trends and Indicators Analysist commenced with the bald fact that we face the twin crises of climate and biodiversity issues, referred to the IPBES drivers for biodiversity loss, and emphasised that we need monitoring if we are to tackle these threats. “Indicators”, he explained, “let us monitor changes in Scotland’s species, habitats and landscapes, and reflect wider changes in the natural environment.”

Making best use of robust indicators was very much part of Simon’s presentation and he explained the value of a set of ‘Smart’ objectives, measuring specific, measurable, achievable, relevant and time bound elements.  He then took us through some of the trends that have caught his eye, one of which was that warmer summers may cause short-term butterfly increases in Scotland but that this increase probably won’t continue in the face of increased frequency of drought and fires resulting from climate change. Simon rounded up by acknowledging the role of citizen scientists.

We headed over to the Netherlands for our sixth presentation as John Smit, of the European Invertebrate Survey, introduced a talk about the Dutch Bumblebee Monitoring Program.  John acknowledged that there was a lot of data in the Netherlands, such as the citizen science portal – waarneming.nl, but he conceded it was ‘just not the right data’.

He explained that their goal was long-term data, gathered to a standardized protocol and gathered nationwide. The Netherlands, he informed us, has 24,000 insect species, over 1,000 of which are pollinators, with 370 of them comprising bees. Clearly that posed a challenge, and thus a decision was made to focus on the 22 species of bumblebee. The advantage of this approach is that bumblebees are relatively easy to find, common in many habitats, and ‘fluffy and cute’, which helps in getting wide public involvement. On the reverse side of the coin are challenges such as difficulties around identification, not being feasible to handle, and the fact that even willing volunteers usually need training.

As with other schemes in Europe, the Netherlands project used existing Butterfly Monitoring Programmes as a springboard, a particularly useful tactic as bumblebees and butterflies were roughly found in the same habitats at the same time of year. Good communication is key to engaging people, and a sequence of excellent bumblebee drawings were among the highlights of John’s session.

A five-year pilot has now ended and John stressed the value of sharing results. Tactics employed included publishing articles online, harnessing the reach of social media and networking, regular volunteer meetings, frequent lectures and newsletters.  The good news is that the pilot has resulted in the monitoring work being absorbed into the official Dutch Ecological Monitoring network.

We wrapped up our event with a presentation from Petra Dieker from the Thuenen Institute of Biodiversity. Petra began by explaining that many of the 590 wild bee species recorded in Germany are found in agricultural landscapes, and that in Germany around 50% of the land mass is used for agriculture. Hence a focus on monitoring in an agricultural setting made perfect sense.

Work began with a four-year pilot scheme to create a nationwide data base describing changes to wild bee populations and their habitats. From this it is anticipated that identifying potential biodiversity-enhancing measures will follow. Such an ambitious project required a substantial team of trained volunteers, in particular farmers.

The method was interesting and adopted a non-lethal approach in sampling. Bee houses, or ‘nesting aids’, were installed at sites across German with a view to attracting bees that nest in cavities..  The 25-storey nesting aid provided a valuable source of data: nesting material, eggs, larvae and, of course, adult species all being observed by volunteers.

Petra’s answer to the question “Could trained volunteers identify nesting aids inhabitants themselves?”  was a resounding “Yes”, with over 90 percent of their recording being correctly identified. 

Petra also discussed a series of bumblebee identification courses which have been benefitting from the creation of small pollinator gardens. These are popular with pollinators and the feeding insects are more or less at eye-level and thus easy to observe. 

The conference was over in a flash, always a sign of things going well, and the feeling was that this was the best we have hosted to date. If it was, then that’s thanks to a stellar line up of presenters, each and every one of whom had a captivating story to tell, and told it brilliantly.

Useful links:

You can follow the work of our presenters and their organisations across various social media and digital channels.

Anthony McCluskey and Butterfly Conservation = www.butterfly-conservation.org/recording and email by amccluskey@butterfly-conservation.org 

Richard Comont and Bumblebee Conservation Trust work = www.beewalk.org.uk, follow Richard on twitter @RichardComont.  In addition details of the Skills for Bees projects can be found at https://www.bumblebeeconservation.org/skills-for-bees-scotland/ 

Claire Carvell and the UK PoMS Team = poms@ceh.ac.uk and @PoMScheme, @Claire_Carvell.  Keep in touch with PoMS updated @ https://ukpoms.org.uk/subscribe

Martin Harvey = Dipterists Forum online and follow Martin on twitter @ kitenet and the Biological Recording Centre @___BRC___. also follow @PoMScheme on twitter too.

Also https://royalsocietypublishing.org/doi/10.1098/rspb.2020.0508 and https://esajournals.onlinelibrary.wiley.com/doi/10.1002/eap.2859  and 

Simon Foster = follow the Trends and Indicators work at Nature Scot via https://www.nature.scot/information-hub/indicators-trends/scotlands-indicators

https://sustainabledevelopment.un.org

https://nationalperformance.gov.scot/measuring-progress/national-indicator-performance

John Smit and EIS Nederland = https://www.eis-nederland.nl/veldtabellen

Petra Dieker = find out more on the website @ https://wildbienen.thuenen.de and follow Petra on twitter at @PetraDieker

Unarmed and dangerous

By Athayde Tonhasca

While the bees discussed last week resort to chemical warfare, the majority of stingless bees have nothing of the kind to defend themselves. The South-American Trigona spinipes is a good template for the behaviour of a great number of little known species in this category.

Don’t mess with me: a T. spinipes stingless bee © José Reynaldo da Fonseca, Wikimedia Commons.

In lieu of a stinger, T. spinipes has five sharp teeth in each of her mandibles; any aspiring nest invader – mostly other bees and ants – will be mobbed, harassed and bitten relentlessly. A colony could be over 100,000-strong, an order of magnitude larger than the size of honey bee colonies. So a T. spinipes swarm is capable of inflicting a lot of painful pinches. And biting has one advantage over stinging; is not as metabolically expensive as producing venom.

These bees often coordinate their attack; some of them clasp their legs around the intruder while others go for the victim’s sensitive parts such as antenna and neck. T. spinipes is not deterred by gigantic trespassers: people lolling about can be nastily surprised by a cloud of perky assailants that dispense painful and persistent bites, get into their nostrils and ears, and tangled in their hair. 

Considering its success in discouraging enemies at home, T. spinipes has the wherewithal to apply its blitzkrieg strategy in other situations; for example, when looking for food. And it does exactly that. It attacks and drives away other bees fancying the same flowers, and is not put off by its opponents’ size; T. spinipes has been observed biting off legs, antennas and wings of honey bees and carpenter bees (Xylocopa spp.). Just the sight of dead Trigona specimens on flowers is sufficient to convince carpenter bees to look for food somewhere else (Sazima & Sazima, 1989).

Mandibles from some stingless bee species. The pain caused by biting is shown on a scale, where 0 = no bite, 1 = biting was visible but could not pinch skin, 2 = able to pinch skin but caused no pain, 3 = mild pain, 4 = moderate pain, and 5 = sharp pain and capable of breaking skin if persistent. All pictures to same scale © Shackleton et al., 2014.

Some stingless bees don’t even bite, or their bites are too weak to cause any harm. But that doesn’t make them less effective. Inexperienced nature-lovers, emboldened by bees’ small size and apparent vulnerability, get too close to a nest only to make a run for it, screeching like banshees despite not receiving a single sting or bite. Naturalist and biologist von Ihering (1883-1939) described an encounter with an unidentified species of stingless bee nesting behind a wall: ‘We knew the bees would attack us, but we were also sure we would not be harmed, exactly, if we resisted the defenders’ petulance. We covered ourselves with a lot of cloth, put some cotton in our ears and started to demolish the brick wall. Countless bees clung to the cloth and everything buzzed around us; some of the attackers managed to reach our face, others, through the back of the neck, reached the neck and hair. No sensation of pain, but an unspeakable irritation […]. Suddenly, without knowing what we were doing, we realized that our legs had taken us away, running fast. The biologist was defeated by the unarmed bees, who the countryman himself respects, because he doesn’t know how to resist to them either’ (Ihering, 1930. Biologia das abelhas melíferas do Brasil).

All these defensive strategies are costly: many bees die when their victims defend themselves. If we were attacked, we would have to pull away chunks of bees to dislodge them from our hair, ears and nostrils. Such kamikaze tactics are not unusual among social insects; Johnson & Hubbell (1974) recorded 63% mortality for three colonies of T. corvina after a two-day battle over sucrose baits. Honey bees detach the stinging apparatus from their bodies (autotomy or self-amputation), which helps in maintaining the injection of venom and the release of alarm pheromones after the stinging action. But sisterly self-immolation is of little relevance to the colony, as long as queens and progeny are protected.

The antics of O. tataira,T. spinipes and other easily irritated stingless bees may give the impression that this lot is all bad news, but far from it: they contribute to the pollination of about 90 crop species (Heard, 1999), and the breeding and management of some of the more docile species have been practiced for centuries by native peoples in Central and South America. The activity, known as meliponiculture, is growing in economic importance, particularly for rural and native communities in Latin America, Africa and Australia. 

L: Nest entrance of Tetragonisca angustula, one of the most reared honey-producing stingless bees in Latin America. R: honey pots from a commercial nest. The flavoursome and aromatic honey is a source of income for countless families.

Why are some stingless bees such bullies? Scarcity of resources and predation pressure are the most likely factors to explain it. Tropical and semi-tropical habitats can be harsh for bees: nectar, pollen and nesting sites are scarce and highly seasonal, and predators, particularly the ubiquitous ants, are a constant menace (Janzen, 1971). In such environments, aggressiveness is a vital survival strategy. Even bees known to us to be mild-mannered such as bumble bees show a Mr Hyde side in the tropics. B. pullatus, native to Central America, and the South American B. morio are notoriously bellicose. Adding to the bad attitude, the venom of B. morio is particularly nasty: people stung repeatedly have been made seriously ill or, on rare occasions, killed.

Despite being bad-tempered, B. morio is an excellent pollinator © Leonardo Ré-Jorge, Wikimedia Commons.

When we stop to watch bees lazily visiting flowers in a garden or park, we may not think about the hazards they face back at home. By storing nourishing food and producing lots of juicy eggs, larvae and a nutrient-rich nest in the case of social species, bees whet the appetite of a variety of looters. They could be ants in the tropics, badgers (Meles meles) in Britain, and countless others. Fleeing or moving away are not options. Survival entails mobbing and scaring your enemies away, poisoning them, or suicidally biting them to death. Whatever it takes for protecting the colony. And life goes on.

An intimidating gang of stingless bees © Bernard Dupont, Wikimedia Commons.

Enlightened approaches in Edinburgh

As summer gathers momentum Edinburgh assumes centre stage for many Scots and visitors alike. The first Edinburgh Festival was held in 1947 and is now an international magnet, the stunning architecture of our beautiful capital city draws people in ever increasing numbers, and who can ignore the history offered at Edinburgh Castle, the mesmeric National Museum of Scotland and the fascinating National Library of Scotland.  And yet if you need to escape the throng you can, and where better to head than Edinburgh’s Royal Botanic Garden?

If you do you will surely be impressed by the visually stunning pollinator-friendly offering. With popular annual and perennial meadows in their care the team at Edinburgh’s Royal Botanic Garden (RBGE) are ideally placed to soothe the soul and help our capital’s pollinating insects.  Add to the mix exciting work with Biodiversity Genomics Europe, and it’s clear to see that pollinators enjoy a healthy focus within their work.

Kirsty Wilson is the Herbaceous Supervisor at RBGE and is particularly well placed to talk about all things meadow-related, which of course brings her into close contact with pollinators.

“First up I should highlight that we have annual and perennial meadows at RBGE,” explains Kirsty. “With our annual meadow we have a well-practiced routine now.  To prepare the ground we kill off unwanted grass and rotivate the soil to create a good weed free seed bed. We then sow our pictorial meadow seed, and after 8 weeks the annual meadow usually starts flowering and continues thereafter until the first frosts.”

“Our annual meadow is both colourful and a great nectar and pollen source for pollinators,” notes Kirsty. “That’s one of the reasons why last year, and again this year, Edinburgh University have been in the garden doing a Bee Foraging Survey.

Annual Summer Meadow outside The Botanic Cottage at Royal Botanic Gardens Edinburgh. The wild flowers are a great source of nectar and pollen for the city’s bees. June 26 2021

“From our perspective it has another welcome bonus. It’s very low maintenance and the flowers change as the weeks go on through the summer lasting until the first frosts. If a visitor was to ask which is the best example at RBGE then I’d probably plump for the ‘ classic mix’ from Pictorial Meadows which you can see outside the Botanic Cottage in the Demonstration Garden this summer.”

RBGE provides a great opportunity make comparisons between the results and methods which underpin annual and perennial meadows. “Our approach to the perennial meadow starts off in similar fashion in that we prepare the ground by killing off weeds and rotivating the soil to achieve a nice even seed bed. It is important to seed with a good native source which is ultimately best for biodiversity. Scotia seed can nevertheless have a range of perennial meadow seed depending on your location and design preference. 

“If all of this seems like too much work you can also go down the increasingly popular route of just sowing yellow-rattle (Rhinanthus minor) by scattering in the yellow-rattle seed in autumn onto the area of meadow you want to create. This is a parasitic plant and will weaken the existing grass, which will then allow you to sow wildflower seed or plant wildflower plug plants of your choice. 

“Typically a good perennial wildflower meadow can take years to establish so patience is key,” concedes Kirsty.  “A perennial meadow will come back each year, but will require an annual cut – typically around the end of August or into September. It is also best to remove the cut grass … as you want the soil to be low in nutrients to allow wildflowers to establish. Better still, if you have sheep, horses or cows allow them to graze it at this time of year, but I appreciate that not everyone will have access to livestock. Another traditional option is to go down the route of using a scythe.

Living lawn

There is another meadow development which Kirsty has seen up close and can point visitors to. “If you are visiting RBGE why not have a look at the native meadow near the poly tunnel in the Demonstration Garden. This is the instant method. This uses pre-grown turf, ideal if you want a fast-established wildflower meadow. However, whilst this does speed up the process it can be expensive – we don’t have this in garden but could suggest it as an instant meadow technique if you have the funds.”

Kirsty’s colleague, Andy Griffiths, is the Sample Coordinator and Field Biologist at RBGE and like Kirsty he too has a keen interest in pollinators. 

“We are a lead partner on Biodiversity Genomics Europe (BGE). One major strand of this project will build a curated European DNA barcode reference library for pollinators, a vital resource to improve biomonitoring and help reverse biodiversity loss. RBGE’s most direct involvement with the pollinator side of BGE will come next year as part of a large-scale malaise trapping case study looking at agricultural intensification.”

The malaise trap that is currently up at RBGE

If that lies in the future Andy is able meantime to point to current activity that is providing an insight into pollinator activity. “We have already started running malaise traps at the RBGE Edinburgh and RBGE Benmore as part of Wellcome Sanger Institute’s Bioscan for Flying Insects project. This UK-wide project uses DNA barcoding to characterise insect genetic diversity over space and time. Perhaps some new pollinator species records for RBGE gardens are waiting to be revealed.”

Not everyone of course is fired by meadows; some are torn between creating habitat and not wanting to go with a full on wildflower meadow approach.  Kirsty has a potential solution for those in the gardening community who might feel that way. 

“Our Living Lawn meadow is perfect if you want to have the look of a neat traditional lawn but want to help wildlife at the same time,” she notes. “It is kept at a height of 10cm tall, and is cut using a lawn mower every two or three weeks. This is perennial, meaning once sown it will come up year after year, and it will be full of wildflowers that are able to grow at a low sward height.”  Kirsty advocates that to plant a living lawn you follow many of the preparation steps that apply to annual and perennial meadow work.  “Best sown in spring or autumn, remember to keep it well watered until established.  Other than that the steps follow the tried and trusted routine of preparing the ground by removing weeds and killing off the grass, then rotivate the soil and once more prepare a nice seed bed for sowing. – having wildflower native species is really good for biodiversity – flowers adapt to flower at a low sward height – we got our living lawn mix from Scotia Seed. 

The RBGE can trace its roots back to 1630, and around a century later Edinburgh found itself embracing the excitement of the Scottish Enlightenment. The latter was a movement of great distinction and achievement heavily reliant on both observation and experiment such as that displayed by the RBGE. It seems reasonable to suggest that their current work on meadows and encouragement of the study of pollinators is just one facet of upholding that fine tradition.

Acknowledgement: With sincere thanks to Alexandra Davey, Andy Griffiths, and Kirsty Wilson at RBGE for providing the information and images for this short blog.

No pasarán

By Athayde Tonhasca

Between 150 and 200 million years ago, some ancestors of today’s wasps (order Hymenoptera) experienced a momentous transformation. The females’ ovipositor – the egg-laying apparatus – evolved into a stinger that produces a cocktail of chemicals capable of paralysing or killing prey and enemies; egg-laying was moved to an opening at the base of the stinger (you can learn details of this evolutionary tale here). By weaponising their ovipositors, those primitive wasps gained a tremendous boost; they could hunt, forage and defend themselves much more efficiently. The venom-injecting lineage flourished, and today comprises over 70,000 species of ants, bees, and stinging wasps known collectively as the Aculeata (derived from the Latin aculeus, meaning barb, thorn). Some of the most successful organisms on Earth are aculates; ants are the main movers and shakers in almost every terrestrial ecosystem (Hölldobler & Wilson, 1990), while bees are the most important pollinators of flowering plants.

A wasp stinger, with a droplet of venom on its tip. The oviduct that carries eggs to the outside is at the base of the stinger © Pollinator, Wikimedia Commons.

Many people’s attitude towards honey bees (Apis spp.) and social wasps such as hornets (Vespa spp.) is of wariness, if not downright hostility, because of their stingers. But these weapons, despite being unpleasantly effective and potentially dangerous to people and animals, are rarely deployed when bees and wasps are flying about. Most stings happen when these insects are handled, or unintentionally squeezed or trapped. Otherwise, they carry on with their busy lives, ignoring us. 

The venom system of the violet carpenter bee (Xylocopa violacea) © von Reumont et al., 2022. 

The mood changes, though, when they feel their homes are being threatened by a raider. The nest is their main reason for being: it harbours the reproductive queens, their young, and food stores. If its walls are breached, in no time the nest would be overcome by parasites, predators and usurpers, and that would be the colony’s demise. So bees and wasps rely on their stingers to fend off enemies, and few wannabe looters can endure the onslaught of hundreds of tiny, poisonous flying daggers.     

Animals tend to keep their distance from the honey bee’s stinger, a sharp, barbed stiletto loaded with venom. L: a beehive fence to keep elephants from farms in Kenya © Kengee8. R: some creatures put up with bees’ wrath for the nutritional rewards of their nests. Art by Ernest Howard Shepard, 1926. Wikimedia Commons.

Despite its efficacy as a defensive mechanism, the stinger is used sparingly. Animal venoms are protein-rich, complex chemical mixtures and therefore metabolically expensive. So bees, wasps and other aculeates can’t afford to go stinging willy-nilly. Some bees reduce the need to sting by making their homes hard to find. You may watch bumble bees (Bombusspp.) time after time in a garden or local park and never find their nests. Other bees use the same tactic of discreet living for protection.

Living inconspicuously for safety. L: a common entrance to several nests of the chocolate mining bee (Andrena scotica) in a busy street. R: nest of Scaura latitarsis inside a termite mound at the top of a tree, 5 m above the ground; A: diagram of the nest; B: entrance; C: detail of the entrance gallery; En – entry; Tm – termite mound; Gl – entrance gallery; Fc – brood combs; En – honey and pollen pots © Camargo, 1970.  

Possessing a stinger sounds like an essential feature for social bees, but a whole group of them do without one: the stingless bees, or meliponines (tribe Meliponini). Stingless bees comprise over 600 species spread around tropical and subtropical regions of the world, but mostly in South America. They have vestigial stingers, so are unable to sting. You may think the lack of a functional stinger makes them defenceless and vulnerable: you would be wrong. 

Some species resort to simplified but no less effective stinger substitutes. The tataíra (Oxytrigona tataira) from South America and similar species secrete large quantities of highly caustic formic acid from their cephalic glands, which is excruciatingly efficient in discouraging enemies, man or beast. The defensive power of O. tataira, named after the Tupi-Guarani tata (fire) and ire (bee), explains its alternatives epithets of cospe-fogo (fire spitter) and the charming caga-fogo(you will need to look up this one). 

An innocent-looking tataíra © Clara Matos, and the consequences to an obstinate man on a mission to destroy a tataíra nest in his small holding, only to be mobbed by angry bees. Two painful weeks later, the man was back on his feet and wiser © Morais et al., 2020.

Other stingless bees deploy less hurtful weapons (at least to us). The sugarbag bee (Tetragonula carbonaria), an endemic Australian species, defeats invading small hive beetles (Aethina tumida) by mummifying them alive. This beetle, a serious pests of the European honey bee (A. mellifera) in some countries, adopts a ‘turtle posture’ to protect itself from bites and stings once inside a bee nest. But the beetle is being too clever by half; the sugarbag bee coats and immobilises the invader with a gloopy mixture of resin, wax and mud. This pharaoh’s approach (Greco et al., 2010) is known as social encapsulation, and it’s practiced by other bees.

A sugarbag bee © James Niland, and a small hive beetle © James D. Ellis, University of Florida, Bugwood.org, Wikimedia Commons.

To survive, insects have to defend themselves against the many dangers in the big wide world. They may run or fly away, hide, or escape detection by crypsis (blending in with the surroundings). But for many bees, wasps, ants and other insects that live in colonies, there is no other option but to stand their ground and fight back – which they do superbly with chemical weapons. Even though, some social bees do very well with no stings or venom. Like The Perils of Pauline, to be continued…

The Perils of Pauline, 1914. Art by unknown author, Wikimedia Commons.

The body snatchers

By Athayde Tonhasca

Family feuds abound in history and in the tabloids, but things got really out of hand with the offspring of Egyptian gods Geb (Earth) and Nut (sky). As the first-born, Osiris was naturally chosen to be the ruler of the world. But his brother Set didn’t care one bit for this undemocratic arrangement, so he decided to despatch Osiris to the Underworld. Set set out a murderous plan worthy of an Agatha Christie story; he commissioned a beautiful casket, tailored to fit a body with Osiris’ exact measurements. Set then organised a magnificent banquet, inviting heavenly celebrities and bro Osiris. When they were all done with the eating and drinking, Set announced a surprise. The casket was brought in, and the host told his guests that whoever could fit inside, could take it home (an odd gift to us, perhaps, but who are we to judge Egyptian gods?). One by one the guests climbed into the casket, which was too small or too big – until Osiris had a go at it. He laid down inside the casket, which, to his glee, fit him perfectly. Set’s trap was set; he slammed the casket’s lid shut and locked it, killing his sibling. Later Set retrieved Osiris’ body and chopped it into small pieces.

The Mummy (1932) escaped from his sarcophagus, but no such luck for Osiris. Art by Karoly Grosz, Wikimedia Commons.

Set’s shenanigans were the perfect inspiration for naming a new species from the genus Euderus, a small group of parasitic wasps in the family Eulophidae. Most Euderus species are moth and beetle parasitoids, but the wasp discovered by Egan et al. (2017) in Florida (USA) is peculiar, to say the least. Its host, Bassettia pallida, is itself a parasitic wasp, but of a different kind: this species is one of the many gall wasps or cynipids (family Cynipidae), which lay their eggs in oaks (Quercus spp.) and less commonly in related plants (family Fagaceae). The egg-laying induces the plant to produce a gall, which is an abnormal growth resulting from increased size or number of cells (galls can also be caused by tissue feeding or infections by bacteria, viruses, fungi and nematodes). Cynipids trigger their host plants to produce nutritious tissue inside their galls, which become ideal places for a larva to grow: there’s nothing better for one’s survival than a cosy, safe and nourishing nursery.

Oak galls or oak apples, growths resulting from chemicals injected by the larva of gall wasps © Maksim, Wikimedia Commons.

In the case of B. pallida, it induces the formation of galls inside stems of sand live oak (Q. geminata) and southern live oak (Q. virginiana). Each of these galls is called a ‘crypt’. So appropriately, B. pallida is known as the crypt gall wasp. When the adult wasp completes its development, it chews an exit hole from inside its woody quarters and flies away.

(a): a crypt gall wasp; (e): adults’ exit holes © Weinersmith et al., 2020.

Life looked good for the crypt gall wasp in the southeastern United States – until we learned about the machinations of its recently discovered enemy. The Eulophidae parasitoid locates a crypt and pierces it with its ovipositor, laying an egg inside the chamber, near or into the developing crypt gall wasp. We don’t know exactly what goes on inside the chamber, but the outcome is not good at all for the crypt gall wasp. When it tries to chew its way out, it’s no longer able to create a hole big enough to fit its body: the wasp becomes entrapped inside its crypt, Osiris-like. During its failed attempt to get out, its head blocks the exit hole. All the better for the parasitoid larva that hatched inside the crypt: it can feed at leisure on the host’s weakened body. On completing its development, the adult parasitoid wasp chews through the host’s head plug and comes out to the big wide world. So there was no better name for this species than Euderus set, the crypt-keeper wasp.

(c): a crypt-keeper wasp pupa in a chamber made by a crypt gall wasp; (f): an exit hole plugged by the head capsule of a dead or dying crypt gall wasp; (g): a crypt gall wasp head capsule chewed through by an exiting crypt-keeper wasp © Weinersmith et al., 2020.

The relationships between oaks and these wasps are examples of host manipulation, which happens when a parasite influences the host’s behaviour or physiology to its (the parasite’s) advantage. The crypt gall wasp induces its host plants to produce galls for its benefit, and in turn the crypt-keeper wasp forces its host into becoming trapped and an easy meal for the parasitoid’s larva: the manipulation of a manipulator is known as a hyper-manipulation, an uncommon phenomenon.

A female crypt-keeper wasp, a hyper-manipulator © Egan et al., Wikimedia Commons.

There are many cases of host manipulation, and the zombie-ant fungus described by the co-author of the theory of evolution by natural selection Alfred Russel Wallace (1823-1913) is one of the better known. This fungus (Ophiocordyceps unilateralis) induces its host ants to climb up the vegetation and clamp their mandibles around a twig or leaf vein. An infected ant will stay put, rain or shine, while the fungus grows inside it. After 4-10 days the ant dies, the fungus grows a ‘stalk’ (stroma) from the ant’s head and releases spores that will infect ants walking about on the forest floor.

A dead Camponotus leonardi ant attached to a leaf vein. The stroma of a zombie-ant fungus emerges from the back of the ant’s head © Pontoppidan et al., 2009.

The more researchers look into it, the more they find cases of host manipulators such as the Darwin wasps Hymenoepimecis spp., which parasitize several species of orb-weaving spiders in the Neotropical region. A female wasp stings and temporarily paralyses her victim, laying an egg on its abdomen. The emerging larva bites through the spider’s cuticle and feeds on its ‘blood’ (haemolymph). The spider carries on with its life, building webs and catching prey, but the growing parasitoid takes its toll; eventually it kills its host. 

L: A H. heidyae egg attached to a Kapogea cyrtophoroides. R: Third instar H. heidyae larva feeding on a recently killed spider; the inset shows details of the dorsal hooks used by the larva to cling to its host © Barrantes et al., 2008.

But shortly before the spider’s demise, somehow – probably by hormone injection – the larva takes command of the host’s behaviour. The spider builds a cocoon web made of thickly woven silk, which doesn’t look at all like a normal web. The spider dies, the larva enters the cocoon and completes its development. Some days later, the adult wasp emerges and flies away.

a. A normal K. cyrtophoroides web; b. The web’s hub; c. A cocoon web induced by the parasitoid;
d.Central section of the cocoon web and the wasp’s cocoon © Barrantes et al., 2008.

Parasitic wasps are not deterred by the defences of hosts such as Anelosimus eximius. This is one of the few species of social spiders; they build massive tent-like nests that shelter hundreds or thousands of individuals, who hunt together in raiding packs and even cooperate in raising their young (watch their comings and goings). But in the Amazon region, A. eximius can’t evade the Darwin wasp Zatypota sp. A parasitized spider leaves the colony and builds its own cocoon-like web. It then becomes immobilised, so that the wasp larva can unhurriedly consume it. When finished with its meal, the larva enters the cocoon to complete its development. The larger the spider colony, the more chances of being parasitized; up to 2% of individuals become hosts to the parasitoid (Fernandez-Fournier et al., 2018).  

L: A group of A. eximius in a communal web © Bernard Dupont, Wikimedia Commons. R: A 5-m long, 3-m high colony of A. eximius; photo by A. Bernard © Krafft & Cookson, 2012.

A fierce looking H. neotropica and its larva feeding on an Araneus omnicolor © Sobczak et al., 2012.

Host manipulation seems to be much more common than we thought, so we shouldn’t expect pollinators to be safe from it. And they are not. The conopid fly (family Conopidae) Physocephala tibialis forces bumble bee hosts to bury themselves in the soil just before dying. The nematode worm Sphaerularia bombi, found throughout the northern hemisphere and South America, infects queens of several bumble bee species, castrating its host. And at least for the buff-tailed bumble bee (Bombus terrestris), the nematode also alters the bee’s behaviour (Kadoya & Ishii, 2015). An infected queen feeds normally, but does not breed or build a nest. Instead, she keeps flying into the early summer months, and by doing so she unintentionally helps to spread the nematode. Certainly many other cases of pollinators’ manipulation by parasites wait to be discovered because their effects can be subtle and inconspicuous.

CSI Garden: a post-mortem examination of a buff-tailed bumble bee found dying on a roadside pavement in England revealed an infestation by the host manipulator S. bombi © The Encyclopedia of Life.

Host manipulation can be seen as a form of extended phenotype (Dawkins, 1982; phenotype refers to a species’ observable characteristics resulting from the expression of its genes). By changing the host’s behaviour for its own benefit, the parasitoid – ultimately, its genes – expresses its phenotype in the world at large. In Dawkins’ own words, ‘an animal’s behaviour tends to maximize the survival of the genes “for” that behaviour, whether or not those genes happen to be in the body of the particular animal performing it’. The phenomenon would have deep consequences for natural selection, but the extent of extended phenotypes has been debated since the publication of Dawkins’ book. 

If you are smugly assuming that behavioural puppeteering is for lower animals such as insects, you’d better think again. Some studies suggest that rodents infected with the protozoan Toxoplasma gondii become more active but sluggish in reacting to alarm signals; worse, they may become attracted to the smell of cat’s urine. If so, an infected mouse has a good chance of prematurely ending its days in a moggie’s maw – which was T. gondii‘s ‘intention’ all along, since cats are its ultimate host. And the plot thickens: infected cats excrete T. gondii spores in their faeces, which can make their way into other mammals. A 26-year study with grey wolves (Canis lupus) from Yellowstone National Park, Wyoming, USA, revealed that infected individuals – probably the result of contact with pumas (Puma concolor) – are bolder, more likely to become pack leaders and have better chances of reproducing (Meyer et al., 2022). In humans, toxoplasmosis, the infection caused by T. gondii, is widespread but usually does not have any symptoms. Most people don’t even know they have it, but all sorts of behaviour and mental disorders such as heightened aggression and Parkinson’s disease have been linked to the infection. The effects of T. gondii on rodents and humans have been disputed because data often show weak, inconclusive or no effects (Johnson & Koshy, 2020). In any case, our invulnerability to the manipulative power of parasites should not be taken for granted. Rephrasing the quote misattributed to Margaret Mead, always remember that in biology, Homo sapiens is unique. Just like every other species.

Invasion of the Body Snatchers (1956). Art by Allied Artists Pictures Corporation. Wikimedia Commons.