Hanging baskets

Ants grow plants in tree nests

Well-maintained ant garden of Camponotus femoratus and Crematogaster levior

Some ants have ant gardens. In their nests, one or more plant species are flourishing. The ants are good gardeners, as a Brazilian research team shows: they select the plants carefully and protect them.

In the forests of the Amazon region, you can see hanging baskets, balls from which plants grow. They are the nests of ants that live in trees. These ant gardens  benefit both parties. The plants belong to species that do not root in the soil but grow on tree branches (or in an arboreal ant’s nest), so-called epiphytes. They benefit because the ants disperse the seeds and fertilize the plants that germinate. The ants benefit because the plant roots strengthen the nest and make it rainproof.

Most of the hanging gardens in the Amazon region belong to two ant species that live together: Camponotus femoratus and Crematogaster levior. They share nests and foraging trails but keep their broods separated. A Brazilian research group describes how well this ant duo takes care of their gardens.

Division of tasks

The two species have divided the tasks. Crematogaster levior goes out to get food. The researchers think that it also is the one that, within a colony, takes the initiative to create a new nest; a colony contains on average 17 nests. Crematogaster levior workers are in the majority, especially in young nests; in initial nests, they are even the only ones.

But Camponotus femoratus is the stronger and more aggressive of the two. He constructs and defends the nests.

This species is also the one that collects seeds of the desired plants and puts them in the cardboard nest wall. He is picky: of the many epiphyte species that grow in South America, the ants only use a handful. Only one or two species are grown per nest.

The most common garden plant is Peperomia macrostachya. Probably, the ants are fond of it because, in addition to nectar glands, flowers and fruits, it also has oil glands. Oil is a hard-to-find part of the diet, so these glands are valuable. Among other plants used are Philodendron species.

Maintenance of ant gardens

The ants take good care of the plants. If a leaf is damaged, experiments showed, workers of Camponotus femoratus will gather there; they are triggered by volatile substances that are released upon damage. So, they arrive at places where herbivore insects are gnawing and they can chase them away. Especially damage to the precious Peperomia macrostachya provokes a rapid influx of many workers.

In addition, the ants prune ‘weeds’. The walls of an ants’ nest are an attractive growing place for many epiphytes because they are rich in nutrients. But the ants prevent the growth of unwanted plants that would compete with the garden plants. If the wrong seeds stick to the wall, the ants will remove them, and if the wrong plants germinate, they will cut the stem or leaves.

No wonder that the garden plants flourish and the hanging baskets look good.

Willy van Strien

Photo: Garden with Philodendron of the ant duo Camponotus femoratus and Crematogaster levior. ©Ricardo Eduardo Vicente

More about gardening ants: mini garden

Sources:
Pereira, A.A., I.V. da Silva & R.E. Vicente, 2021. Interaction between epiphytic chemical allelopathy and ant‑pruning determining the composition of Amazonian ant‑garden epiphytes. Arthropod-Plant Interactions, online April 9. Doi: 10.1007/s11829-021-09825-5
Dacquin, P., F. Degueldre & R.E. Vicente, 2021. Relative colony size of parabiotic species demonstrates inversion with growth. Insectes Sociaux, online January 2. Doi: 10.1007/s00040-020-00798-x
Vicente, R.E., W. Dáttilo & T.J. Izzo, 2014. Differential recruitment of Camponotus femoratus (Fabricius) ants in response to ant garden herbivory. Neotropical Entomology 43: 519-525. Doi: 10.1007/s13744-014-0245-6

Shrimp keepers

Longfin damselfish have their algal farms fertilized

Longfin damselfish grows algae with help of shrimp

Every intruder is chased away from the algal farm of the longfin damselfish, but a swarm of opossum shrimp is allowed stay and even receives protection. For good reason, Rohan Brooker and colleagues report.

The longfin damselfish (Stegastes diencaeus) is an aggressive, territorial fish that lives on coral reefs. It grows its own food by creating a farm of a few square meters where palatable algae grow. It tends its algae and defends its territory fiercely; all animals are chased off.

Or rather: almost all animals. Rohan Brooker and colleagues show that during the day, a swarm of opossum shrimp (Mysidium integrum) can be found in many algal farms. A farmer not only tolerates the shrimp’s presence, but it also protects them from their predators, although it takes some extra effort. Apparently, the tiny animals are worth it.

Flourishing farm

Why would an algae-farming longfin damselfish care about the shrimp, Brooker wondered. Although the fish supplements its algae diet with some small animals, it does not eat these shrimp. Perhaps, Brooker supposed, the shrimp are fertilizing the algae with their feces.

And that turned out to be the case. A farm with a swarm of shrimp does better than a farm without such swarm, thanks to nutrients excreted bythe shrimp. It hosts more large brown algae that form a structure on which turf-algae, which the damselfish prefers to eat, grow well. This translates into a better condition of the fish: damselfish with a shrimp swarm on their farm have a larger energy reserve than colleagues with a non-fertilized farm.

Brookers conducted his research on coral reefs off the coast of Belize, Central America.

Domesticated

Thus, the farming fish benefits for its flourishing crop, the shrimp for its guarded refuge. There are no shrimp swarms to be found outside farms during daytime. The shrimp leave the farm at night, when it is safe, to filter food from the water at the surface. Then they return to their permanent residence.

The fidelity to this place is so strong that young shrimp remain in their parents’ farm. Therefore, the authors consider the relationship between longfin damselfish and opossum shrimp as an early stage of domestication. The fish ‘keep’ the shrimp as livestock.

Willy van Strien

Photo: Longfin damselfish Stegastes diencaeus. Mark Rosenstein (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

The research explained on YouTube

Source:
Brooker, R.M., J.M. Casey, Z-L. Cowan, T.L. Sih, D.L. Dixson, A. Manica & W.E. Feeney, 2020. Domestication via the commensal pathway in a fish-invertebrate mutualism. Nature Communications 11: 6253. Doi: 10.1038/s41467-020-19958-5

Males parasitizing on females

The immune system of deep-sea anglerfishes is strongly modified

In deep-sea anglerfish, some species have parasitic males and an aberrant immune system

To the well-known peculiarities of deep-sea anglerfish, Jeremy Swann and colleagues add a new one: some species lack an important part of the immune system. This is associated with a unique parasitic lifestyle of males.

There are strange, very strange and extremely weird animals. We can safely include deep-sea anglerfish in the latter group.

Within the anglerfish or seadevils, they form a separate group of over 160 species, the Ceratioidea, which, as the name indicates, have specialized in living in the utter darkness of the deep sea. Food and partners are extremely scarce down there. Hence, as was known, these fish exhibit some peculiarities. Now, it turns out that they also have a very aberrant immune system, Jeremy Swann and colleagues report.

Angling pole with glowing bulb

Deep sea anglerfish start their lives in a quite normal way, eggs and larvae dwelling in surface waters. But once they developed into young fish, things change. Females grow to a considerable size, males stay tiny.

The bigger a female gets, the more eggs she can produce. And so a young female starts growing. She has to eat much, several prey animals are on her menu. To capture prey, she uses a fishing rod growing from her back; it is a modified anterior dorsal fin. At the end it has a lure: a bulb in which bacteria live that produce light by carrying out a chemical reaction. It is a form of mutualism; the bacteria get a place to live in and food in exchange for light production.

An anglerfish’s light can flash and dance, resembling a moving animal. Living animals discern a tasty snack which they will approach. The anglerfish then ingests a large amount of water, including prey. With some luck, the catch will provide sufficient nutrients to sustain her for quite a while.

The females, plump and with large heads and mouths full of sharp teeth, are not the prettiest of all. They are called seadevils for good reason. They are bad swimmers, drifting around, just waiting for prey to come by.

Strong attachment

After completing the larval stage, males’ development takes a completely different direction. Males no longer grow and are unable to eat. Their only goal is to find a female in the empty deep sea. So, they swim constantly. In addition to the light bulb of their angling rod, young females also have two luminous organs on their backs. Maybe the dwarfed males, which have big eyes, are able to detect those organs. If they are lucky, they will meet a partner before they have used up all their reserves.

Upon meeting, he attaches himself to her body with sharp teeth. When, later on, she is ready to release eggs, he is ready to fertilize them. Males and females only become sexually mature when they’ve acquired a partner. Given the scarcity of conspecifics, this makes sense: only after pair formation it is guaranteed that eggs and sperm can come into contact.

Sperm bulge

In some deep-sea anglerfish, the attachment between female and male is temporary; after a while, he lets go.

But in other species, males attach themselves permanently to a female. These are most bizarre types, because the two partners fuse with each other, enabling the male to survive. Their skin tissues meld, the circulatory systems become connected. He now is a ‘sexual parasite’, little more than a sperm-producing bulge that feeds on nutrients that he derives from her. This sexual parasitism is a unique mode of reproduction, occurring only in deep-sea anglerfish.

It is called parasitism, but it may be considered a form of mutualism as well, as the male delivers sperm in return for nutrients.

The best known species is Ceratias holboelli; it is also the largest one and it has the most extreme sexual dimorphism. A female can grow more than a meter long (including tail), sixty times the size of a free-living male. Physical pair formation is permanent. Once attached to her belly, he grows to a maximum of 20 centimetres. A female carries no more than one parasitic male.

Another species with permanent attachment is Cryptopsaras couesii; in this species, up to eight males can be attached to a single female. A female can be 30 centimetres long, a free-living male only three centimetres.

Ancient immune system

It is remarkable that the female immune system doesn’t attack permanently attached, parasitic males, Swann and colleagues realized. You would expect the immune system to recognize and reject such males, as they are not-own tissue. But that does not happen.

Apparently, the immune system tolerates the very intimate mode of reproduction. To find out how, the biologists examined a number of genes that underpin various parts of immune defence. They investigated four deep-sea anglerfish species with temporarily attached males and six species with permanently attached parasitic males, including Cryptopsaras couesii. They compared these species to a number of anglerfish species outside the deep-sea group, where males don’t attach to females.

Fishes have the same immune system as other vertebrates; the system is 500 million years old. It consists of innate, general immune responses on the one hand and specific immune responses that build up against specific intruders that the system has to deal with on the other hand. The researchers focused on the adaptive, specific immune system.

Lethal

The results were surprising: deep sea anglerfish species in which males live as parasites on females lack essential immune genes. Their specific immune system is severely blunted.

In two of the species studied, species in which females can have more than one male attached, virtually no specific immune facilities are functional. This is highly remarkable, because such complete lack of specific immune defence is lethal for other animals. The first infection would kill them. Microbial pathogens occur in the deep sea too, so deep-sea anglerfish must be able to defend themselves. Most likely, they reorganized their innate immune defence, the researchers assume.

From their own and other research, they conclude that the common ancestor of deep-sea anglerfish had tiny, non-parasitic males that temporarily attached themselves to females. On a few occasions, species descending from that ancestor made the switch to permanent attachment and their specific immune defence has been largely dismantled.

It is unclear yet what happened first. Did males become parasitic, making it necessary to turn off the specific immune system? Or did the specific immune system lose important parts, making permanent attachment of males possible?

The deep sea anglerfish remain really puzzling creatures.

Willy van Strien

Drawing: northern giant seadevil, Cryptopsaras couesii (not included in this research); female with male attached. Tony Ayling (Wikimedia Commons, Creative Commons CC BY-SA 1.0)

Watch the fanfin angler, Caulophryne jordani (not included in the research) on YouTube; female with permanently attached male

Sources:
Swann, J.B., S.J. Holland, M. Petersen, T.W. Pietsch, T. Boehm, 2020.  The immunogenetics of sexual parasitism. Science, online July 30. Doi: 10.1126/science.aaz9445
Fairbairn, D.J., 2013. Odd couples. Extraordinary differences between the sexes in the animal kingdom.  Princeton University Press, Princeton and Oxford, VS. ISBN 978-0-691-14196-1

Joint forces against brood parasite

When yellow warbler is warning, red-winged blackbird will attack

Red-winged blackbird eavesdrops on yellow warbler's alarm call

The yellow warbler utters a specific alarm call when a brood parasite is nearby. The red-winged blackbird picks up the signal and attacks, as Shelby Lawson and colleagues write. Together, the birds protect their nests.

Brown-headed cowird parasites on nests of songbirdsA bird’s nest with eggs or young is vulnerable. One of the dangers is that a heterospecific bird will lay an egg in it and charge the parents with the care of a foster young, like the cuckoo does. The red-winged blackbird, which breeds in wet areas in North and Central America, runs such risk. Here the brown-headed cowbird is the ‘cuckoo’, the brood parasite.

Although a young cowbird, unlike a cuckoo chick, does not eject its foster brothers and sisters out of the nest, its presence is to their detriment. The foreign chick demands so much attention that the legitimate young will suffer and starve or fledge in a bad condition.

So, the red-winged blackbird must keep the cowbird out of its nest. It takes advantage of the vigilance of the yellow warbler, another passerine bird that is visited by the cowbird, Shelby Lawson and colleagues show. The yellow warbler, in turn, takes advantage of the aggression of the redwing.

Defense

Yellow warbler utters specific alarm call when brood parasite is presentWhen yellow warblers detect a brown-headed cowbird, they utter a specific alarm signal, a ‘seet’ call. Upon hearing that call, all females respond appropriately: they immediately return to their nest (if they were not already there), repeat the seet and sit tightly on their clutch. As a consequence, a cowbird has no access.

Yellow warblers utter the seet call only in response to the brood parasite and only during the breeding period. To warn of predators, they have a different signal, and upon hearing that call, females will change perches and remain alert, but they won’t return to the nest. The combination of the specific alarm signal for brood parasites and the appropriate response of females is unique.

The researchers wondered whether red-winged blackbirds eavesdrop on that specific signal and take advantage of it. They play backed different sounds nearby redwings’ nests and observed their responses.

Both redwing males and females became aggressive upon hearing the seet of yellow warblers and attacked the speaker. They reacted as heated as in response to the chatter of brown-headed cowbirds. Also the call of a blue jay, a nest predator, aroused their aggression. Apparently, the response to the seet call is a general defence against various dangers that threaten a nest. The birds neglected the song of an innocent songbird.

Chatter of other redwings elicited the strongest defence response; the birds seem to consider conspecifics that invade their territory to be the greatest risk.

Together

The yellow warblers’ signal to warn of brood parasites is picked up by red-winged blackbirds, which respond by approaching the danger. This is to the benefit of yellow warblers: previous research had shown that their nests suffer less from parasitism by cowbirds if they breed in the neighbourhood of red-winged blackbirds. Redwings and yellow warblers often nest in loose aggregations; together they are able to resist the brood parasite.

So far, the red-winged blackbird appears to be the only bird species that understands and responds to yellow warblers’ warning of brood parasites.

Willy van Strien

Photos:
Large: Red-winged blackbird. Brian Gratwicke. (Wikimedia Commons, Creative Commons CC BY 2.0)
Small, upper: Female brown-headed cowbird. Ryan Hodnett (Wikimedia Commons, Creative Commons CC BY-SA 4.0)
Small, lower: Male yellow warbler. Mykola Swarnyk (Wikimedia Commons, Creative Commons CC BY-SA 3.0)
https://commons.wikimedia.org/wiki/File:Yellow_Warbler_Setophaga_aestiva_m_Toronto1.jpg

Researchers tell about their work on YouTube

Sources:
Lawson, S.L., J.K. Enos, N.C. Mendes, S.A. Gill & M.E. Hauber, 2020. Heterospecific eavesdropping on an anti-parasitic referential alarm call. Communications Biology 3: 143 . Doi: 10.1038/s42003-020-0875-7
Gill, S.A. & S.G. Sealy, 2004. Functional reference in an alarm signal given during nest defence: seet calls of yellow warblers denote brood-parasitic brown-headed cowbirds. Behavioral Ecology and Sociobiology 5671-80. Doi: 10.1007/s00265-003-0736-7
Clark, K.L. & R.J Robertson, 1979. Spatial and temporal multi-species nesting aggregations in birds as anti-parasite and anti-predator defenses. Behavioral Ecology and Sociobiology 5: 359-371. Doi: 10.1007/BF00292524

Leaf cutters prevent traffic jams

Take no heavy load when traffic flow is high

leaf cutter ants carry small leaf fragments on crowded trails

When the number of workers on foraging trails is high, leaf cutters maintain the flow by carrying only small pieces of leaf with them, Mariana Pereyra and Alejandro G. Farji-Brener show. Otherwise traffic jams would arise.

The fungus that leaf cutter ants grow in their gardens needs fresh plant material continuously to grow on. And so ant workers walk up and down trails that are cleared and maintained free of debris. They leave the nest to cut leaf fragments from plants and return with a piece in their jaws.

Sometimes ants carry extra-large leaf fragments, causing them to move slowly. That is cumbersome when the trail is crowded, because then a slow ant may hinder the flow. Accordingly, when many ants are walking on the path, they only take small loads with them, Mariana Pereyra and Alejandro Farji-Brener write.

Truck-driver effect

In earlier research, Farji-Brener and colleagues had shown that workers of the leaf cutter Atta cephalotes sometimes carry a strikingly large piece of leaf, up to twice the normal size, to deliver a large gain at the nest. But such extra large burden also has disadvantages; a heavily loaded ant runs slower and hinders the ants that come behind her carrying a normal load. Their walking speed may be reduced by up to 50 per cent. So, a traffic congestion may form behind a heavily loaded worker; the researchers call it the truck-driver effect. It slows down the entire column.

A slow ant on the trail is especially obstructive when it is busy, because in that case, ants walk close together and cannot overtake a slow colleague. At high ant flows, the biologists observed relatively few ants with a heavy load. Is that because the ants are so ‘wise’ not to enter a busy path with a heavy load?

Steady flow

Pereyra and Farji-Brener now answered that question in another species, Acromyrmex crassispinus. They offered workers pieces of ‘leaf’: filter paper soaked in orange juice. They presented pieces of normal size and of extra large size and observed what choice the ants made when different numbers of ants were walking on the trail. And indeed: only at low ant flows, workers selected extra large pieces of paper; when many ants were running, they only picked up the smaller pieces.

Various reasons are thinkable for avoiding large pieces; they make it more difficult to manoeuvre in case of obstacles, the chance of collisions is greater and a heavily loaded ant is more vulnerable to predators. But the fact that ants tend to ignore the large parts at high ant flows suggests that they also do so in order not to obstruct traffic. In this way, leaf cutters optimize colony performance. All going at the same speed: on a busy path, that is the best way to keep a steady flow.

Just like on highway.

Willy van Strien

Photo: Atta cephalotes ©Alejandro Farji-Brener

Sources:
Pereyra, M. & A.G. Farji-Brener, 2019. Traffic restrictions for heavy vehicles: Leaf-cutting ants avoid extra-large loads when the foraging flow is high. Behavioural Processes, online November 25. Doi: 10.1016/j.beproc.2019.104014
Farji-Brener, A.G., F.A. Chinchilla, S. Rifkin, A.M. Sánchez Cuervo, E. Triana, V. Quiroga & P. Giraldo, 2011. The ‘truck-driver’ effect in leaf-cutting ants: how individual load influences the walking speed of nest-mates. Physiological Entomology 36: 128-134. Doi: 10.1111/j.1365-3032.2010.00771.x

The art of pest control

Fungus-growing termites keep their gardens clean

Termites that grow fungus for food manage to keep their crops free from pests, such as weeds, pathogens and fungus-eating nematodes, Saria Otani and Natsumi Kanzaki and their colleagues report. Bacteria in the termites’ gut play a role in pest control.

Some termites species practice agriculture by growing a fungus in their nests for food. And just like human farmers, they have to protect their crop against pests. As is known, they perform well. Saria Otani and colleagues show how a number of African termite species keep their fungal gardens free from non-edible, proliferating or pathogenic fungal species. And Natsumi Kanzaki and colleagues report that the Asian termite Odontotermes formosanus suppresses fungus-eating nematodes.

One way by which the termites control these pests, is by ingesting the plant material on which they grow the fungus crop, so that it passes through their gut. Gut bacteria produce substances that inhibit harmful fungi and nematodes, to ensure that the pre-digested stuff is pretty clean.

Agriculture in termites

Just like ants and some bee and wasp species, termites are eusocial. They live in large colonies that can exist for decades. Most residents are sterile: they are either workers that maintain the nest, take care of the brood and forage for food, or soldiers that defend the nest. Reproduction is a privilege of the royal couple, that has no other duties. The queen is nothing more than an egg laying machine, the king’s task is to mate with her.

Winged sexual individuals (alates) appear once a year. They make a nuptial flight, and couples form that may found a new colony.

More than three hundred species of termites from Africa and Asia have a special way of life: in indoor gardens, they grow fungi in highly productive monocultures. In these species, the workers have the additional task of taking care of the crop. They forage for tough plant-derived material on which they grow the fungus: dry grass, wood and leaf litter. The gardeners consume the stuff and deposit it with their faeces on top of the garden. They are unable to degrade the cellulose and lignin of plants, but the fungus grows well on the pre-digested and fertilized material. It forms nutritious buds, the nodules, which are consumed by the termites. The nodules contain asexual spores, which pass the termites’ gut undamaged; by dropping them on top of the fungal garden, the termites maintain the crop. They also consume older, lower garden parts that are whitish with fungal mycelia.

Cleaning process

Both termite and fungus profit from this agriculture: it is a mutualistic relationship. The fungus has a safe and comfortable living place, the termites have a food supply. But a problem is, that the well attended fungal gardens are suitable as a living place or food source also to other parties.

A garden, for instance, is attractive to fungi that are of no use to the termites, but are competitive with or pathogenic to the crop. The plant material that the workers bring in from the field is not free of such species. Yet, Otani could hardly find harmful fungi in the gardens of three African species, including Macrotermes natalensis. He shows that both the fungal crop and the garden contain substances that inhibit the growth of foreign fungi.

The termites do not synthesize such substances, but their gut bacteria do. By eating the plant material before provisioning the fungus crop, the gardeners probably subject it to a cleaning process. Gut bacteria are deposited on the garden with the faeces, and continue to produce fungicidal substances.

Grooming

Because the fungal crop is full of carbohydrates, proteins and fats, it is an attractive food source for other animals, such as fungus-eating nematodes. Their presence would reduce the harvest. Natsumi Kanzaki shows, in the Asian termite species Odontotermes formosanus, that workers that leave the nest to forage for plant material often carry such nematodes upon return, as does their load.

The fungal crop is not toxic to the nematodes. But they don’t get a chance to eat it, because the termites will groom returning colony mates to remove hitchhiking nematodes. Also, the foragers are not in direct contact with the garden. And when the gardeners consume the new plant material, gut bacteria will suppress nematodes that cling on it.

Obligate

Termite farming originated in Africa. The farming is obligate for both partners: fungi-growing termites and cultivated fungi no longer are capable to live on their own.

Although termites look a bit like ants, they are not related to them. On the evolutionary tree of life, they are close to cockroaches. That is why certain differences exist between termites and ants. Whereas male ants are not engaged in colonial life (all workers are females), sterile male termites help their nest mates as workers or soldiers. Juvenile termites do not go through larval and pupal stages, but are nymphs, small versions of adult animals.

Willy van Strien

Photos:
Large: Odontotermes formosanus, young alates and workers. ©Wei-Ren Liang
Small: Macrotermes natalensis: fungus garden with nodules, soldiers and nymphs. ©Saria Otani

Sources:
Kanzaki, N., W-R. Liang, C-I. Chiu, C-T. Yang, Y-P. Hsueh & H-F. Li, 2019. Nematode-free agricultural system of a fungus-growing termite. Scientific Reports 9: 8917. Doi: 10.1038/s41598-019-44993-8
Otani, S., V.L. Challinor, N.B. Kreuzenbeck, S. Kildgaard, S. Krath Christensen, L. Lee Munk Larsen, D.K. Aanen, S. Anselm Rasmussen, C. Beemelmanns & M. Poulsen, 2019. Disease-free monoculture farming by fungus-growing termites. Scientific Reports 9: 8819 . Doi: 10.1038/s41598-019-45364-z
Aanen, D.K. & J.J. Boomsma, 2006. Social-insect fungus farming. Current Biology 16: R1014-R1016. Doi: 10.1016/j.cub.2006.11.016
Aanen, D.K., P. Eggleton, C. Rouland-Lefèvre, T. Guldberg-Frøslev, S. Rosendahl & J.J. Boomsma, 2002. The evolution of fungus-growing termites and their mutualistic fungal symbionts. PNAS 99: 14887-14892. Doi: 10.1073/pnas.222313099

Healer

Wound heals faster in presence of cleaner shrimp

Cleaner shrimp helps wound healing

In case of injury, fish get extra benefits from the services of cleaner shrimp, David Vaughan and colleagues demonstrate. Even though the cleaner does not specifically clean the wound, its treatment aids healing.

Cleaner shrimp, just like cleaner fish, occupy cleaning stations for fish clients on coral reefs. With their mouthparts, they pick parasites and dead or damaged tissue from the skin of their clients, enjoying a morsel of food: a win-win situation. Such helper is the Pacific cleaner shrimp Lysmata amboinensis, which lives on coral reefs in the Pacific Ocean, Indian Ocean and Red Sea; in the film Finding Nemo, Jacques is representing this species.

How will this cleaner behave to a fish that sustains an injury, David Vaughan and colleagues wondered. Does it take advantage of an injured client by biting off some exposed living tissue? Or might his cleaning treatment be beneficial?

Inflammation

The researchers took cleaner shrimp into the lab, and also a number of sea goldies (Pseudanthias squamipinnis), a fish species that lives around coral reefs. They inflicted a small, superficial wound to one side of some fish, under anaesthesia; in the field, such wounds often occur. Half of the injured fish was then transferred individually to a tank where a cleaner was present for one hour each day; the remaining fish were housed in tanks without a cleaner. For control, uninjured fish were also placed in tanks with or without daily visits of a cleaner shrimp. The behaviour of fish and shrimp was observed, and healing of the wound was monitored.

A fish that wants its skin to be treated, will visit a cleaner shrimp and adopt an inviting attitude, presenting the side of the body it wants to be cleaned. Just after injury, it turns out, fish solicit cleaning less often. They keep the damaged side away from the shrimp.

But within 24 hours, the wound is closed. The spot turns red, indicating an inflammation; the redness increases during the first two days.

A wounded fish that has access to cleaner shrimp now wants to be cleaned at both sides. And after a few days, cleaning turns out to have health benefits: the redness of the wounded site decreases from the second day on, so inflammation subsides. After six days, a clear difference is seen between fish that were cleaned and fish that were not; in the latter fish, the redness has remained high. In other words: thanks to the activities of cleaner shrimp, a wound heals faster. There was no trace of abuse: the shrimp don’t aggravate an existing wound, nor do they cause any new damage.

Positive effect

Cleaner shrimp don’t focus cleaning specifically around the injury site, but treat an injured fish like they treat an uninjured one. The researchers think that the cleaning has an indirect positive effect, by keeping pathogens at bay that would otherwise invade the wound. Moreover, it is known that cleaner shrimp reduce stress in their clients. That will also help the healing process. So, by cleaning, cleaner shrimp also offer healing services.

Willy van Strien

Photo: Bernard Dupont (Wikimedia Commons, Creative Commons CC BY-SA 2.0)

Source:
Vaughan, D.B., A.S. Grutter, H.W. Ferguson, R. Jones & K.S. Hutson, 2018. Cleaner shrimp are true cleaners of injured fish. Marine Biology 165: 118. Doi: 10.4225/28/5b2c885b32331

Help when needed

Crab spider makes itself useful on infested flower

crab spider hunts prey on flowers

Lying in ambush on a flower, a crab spider will grab every visitor and eat it. Its victim may be a useful guest, such as a bee, as well as a harmful one. In buckler mustard, the presence of a crab spider turns out to be beneficial if flowers are infested by caterpillars, Anina Knauer and colleagues show.

Crab spiders have an effective way to acquire food. They reside in a flower, usually inconspicuously as their colour matches that of the flower, and wait for visitors to arrive. They grab them with the two pairs of large legs to which their name refers, kill them with a poisonous bite and eat them. They can handle prey that is much larger than they are. It is a disadvantage for a plant when such a spider settles on a flower, you would guess, for many flower visitors that they hunt are useful visitors, such as bees that pollinate the plant to enable it to set seed; it would be a disaster if those pollinators could not do their job.

But Anina Knauer and colleagues show that the presence of a crab spider can be a blessing. That is because a flower also gets visitors with bad intentions, and a resident crab spider can eliminate them. Therefore, they discovered, a flower will attract crab spiders in case of unwelcome visitors.

Seed set

buckler mustard attracts crab spider if infested by caterpillars
The researchers investigated how the presence of the crab spider Thomisus onustus affects the fitness of the plant it usually occurs on, buckler mustard (Biscutella laevigata), an alpine herb with yellow flowers and fruits that look like spectacles. The plant interacts with several insect species that are potential prey for the spider. The scent of the flowers attracts bees that take care for pollination in exchange for nectar. But the seed setting often fails because the flowers are consumed by caterpillars of the diamondback moth (Plutella xylostella). What happens when a crab spider is present?

The researchers conducted experiments in which they placed three caterpillars on flowers of plants with or without a crab spider every morning and counted the caterpillars in the evening. On plants with a crab spider, most of the caterpillars disappeared – apparently, they were eaten by the spider -, and after four weeks, as a consequence, those plants had suffered much less damage than plants without a spider and developed seeds normally. The crab spider rescued the flowers.

In the field, the researchers also found, plants call the voracious spider for help when the flowers are infested. This call is chemical: infested flowers emit increased amounts of one of the scent compounds, beta-ocimene. The crab spider is attracted by that compound and will settle on such flowers. Indeed, a larger proportion of plants with caterpillars is occupied by a crab spider compared to plants without a spider. So, plant and spider have a mutualistic relationship: an infested plant asks for help and receives it, while the spider that comes to the rescue gets a meal.

Bees

But what about the bees, which are the most important pollinators? Aren’t they in danger when a spider is present? They hardly are, as it turns out. They usually detect the presence of a spider on a flower, despite its camouflage, and avoid a visit, and the spider almost exclusively feeds on caterpillars. Still, despite the reduced visit rates of bees, the flowers set seed. Apparently, there is no lack of pollen. The presence of the spider therefore turns out to be beneficial for plants that are infested by caterpillars.

High in the mountains Thomisus onustus does not occur, while buckler mustard does. Upon attack by caterpillars, plants of highland populations increase the amount of beta-ocimene to a much less extent than plants of lowland populations.

Willy van Strien

Photos:
Large: Thomisus onustus (not on buckler mustard). Paco Gómez (via Flickr, Creative Commons CC BY-SA 2.0)
Small: buckler mustard. Isidre blanc (Wikimedia Commons, Creative Commons CC BY-SA 4.0)

Source:
Knauer, A.C., M. Bakhtiari & F.P. Schiestl, 2018. Crab spiders impact floral-signal evolution indirectly through removal of florivores. Nature Communications 9: 1367. Doi: 10.1038/s41467-018-03792-x

Deceit, abuse and benefits

Complex relationships between arum, blowflies and lizard

Dead-horse arum flower is attractive to lizard

With its smell of rotting carrion, the dead-horse arum Helicodiceros muscivorus is irresistible to blowflies and a lizard. The blowflies will be abused, the lizard benefits. Ana Pérez-Cembranos and colleagues unraveled these complex relationships.

On islands in the Mediterranean Sea, a plant occurs with a very bad smell, the dead-horse arum, Helicodiceros muscivorus. Its odour contains chemical components that are also emitted by a decomposing dead animal. It irresistible to a female blowfly searching for carcasses to lay her eggs on to make sure that the carnivorous larvae will have food. The dead-horse arum takes advantage of that behaviour.

The plants release their odour on the first day of blooming. Blowflies that perceive the smell cannot ignore it. Upon approaching the source, they find a pink or red curved bract, the spathe, with the hairy end of the spadix (inflorescence), which produces the smell. When they land, the spadix turns out to be warm. To blowflies, the imitation is perfect: this is rotting carrion. Guided by the heat, they crawl into the tube that is formed by the base of the spathe around the lower part of the spadix, which bears female and male florets.

Trapped

Once inside, the blowflies don’t find what they need, which is decaying meat. But if they want to leave, they cannot. Spikes on the spadix keep the door closed. The blowflies are trapped.

Unintentionally, they provide a service to the arum during their imprisonment in the floral chamber. The female flowers at the bottom of the spadix are blooming this first day, and blowflies that had been misled by the arum before, now deliver the pollen that they picked up on that occasion. The plant has its female flowers pollinated.

The next day, the female flowers have faded and the male flowers are mature. The stench and the heat disappear, the spikes wilt and the blowflies escape, and while passing the male flowers, they are loaded with pollen. And here is the second benefit to the plant: the blowflies take the pollen with them to female flowers elsewhere – if at least they find another foul smelling arum on their way and are again misled into visiting it.

So, the blowflies are coerced to pollinate the dead-horse arum without receiving any reward such as nectar. On the contrary: they lose time that they should have spent on searching for genuine carcasses.

Basking

Now Ana Pérez-Cembranos and colleagues show that the Balearic lizard Podarcis lilfordi is also misled by the arum’s odour. The animal is omnivorous and sometimes forages on carcasses, which are also attractive as a heat source; lizards are cold-blooded and when the weather is cool, they may use a rotting carcass as a perching site for basking. In addition, they capture the blowflies that arrive at the cadaver in search for a site for oviposition.

The lizards respond to the smell of the dead-horse arum as they do to the smell of a carcass and will approach the source. If that turns out to be a dead-hors arum instead of a dead animal body, they will not find a meat meal, but they do find a basking place and blowflies, which they take from the spathe or grab from the tube. The lizards thus take away a number of pollinators, but, according to the researchers, enough are left to ensure pollination.

Fruits

So, the lizard isn’t an enemy of the arum. And after the flowering period, when fruits are ripe, a mutualism even develops between both. The lizards consume the fruits and disperse the seeds in their faeces; passage through the lizard’s intestine increases the probability of germination. On Aire Island, a the small island off the southeastern coast of Menorca, where the research was done, the dead-horse arum is a newcomer. It is estimated to have grown there for only about fifty years. In that period, it spread rapidly over the island and nowadays it locally occurs in great densities. That is because of the lizard, which has learned to eat the fruits and now is the main disperser of the seeds, the researchers think.

Willy van Strien

Photo: Balearic lizard on the spathe of the dead-horse arum © Ana Pérez-Cembranos

Sources:
Pérez-Cembranos, A., V. Pérez-Mellado & W.E. Cooper, 2018. Balearic lizards use chemical cues from a complex deceptive mimicry to capture attracted pollinators. Ethology  124: 260-268. Doi: 10.1111/eth.12728
Angioy, A-M.,  M. C. Stensmyr, I. Urru, M. Puliafito, I. Collu & B. S. Hansson, 2004. Function of the heater: the dead horse arum revisited. Proceedings of the Royal Society London B 271: S13-S15. Doi: 10.1098/rsbl.2003.0111
Stensmyr, M.C., I. Urru, I. Collu. M. Celander. B.S. Hansson & A-M. Angioy, 2002. Rotting smell of dead-horse arum florets. Nature 420: 625-626. Doi: 10.1038/420625a

Multi-coloured livestock

Thanks to tending ants, mixed aphid colonies persist

Lasius japonicus tending its two-coloured livestock

The aphid milking ant Lasius japonicus ensures long-lasting coexistence of two colour morphs of the mugwort aphid, from which it harvests honeydew, Saori Watanabe and colleagues write. Without intervention, its favourite colour would be displaced.

Like many other ants, the Asian ant Lasius japonicus has a mutualistic relationship with aphids. The aphids suck sap from their host plant and excrete excess sugars, dissolved in a liquid: honeydew. The ant fights off their natural enemies and harvests (‘milks’) the sugary honeydew. One of its mutualistic partners is the Japanese mugwort aphid, Macrosiphoniella yomogicola, which lives on mugwort, a common plant of Europe and Asia. The protection of the ant is of crucial importance to the aphids; each colony will fall victim to its enemies if not protected.

Quality

The mugwort aphid occurs in different colours, with red and green as the most common types; large green specimens will turn black. The ant has a preference for the green morph, Saori Watanabe and colleagues show, because it excretes a higher quality honeydew. But as a consequence, the red morph, which retains a larger proportion of the sugars that it obtains from the host plant, can reproduce at a higher rate. All aphids are females that reproduce parthenogenetically, their young being clones of their mother. Red aphids produce red daughters, green aphids green daughters – and the green morph runs a risk to be displaced by the red one.

But, as it turns out, the ants prevent this from happening. The researchers show that the red aphids indeed are able to multiply faster than the green ones. As a consequence, in laboratory experiments, the proportion of green aphids in a mixed colony decreased, but only if the researchers withheld attending ants. If, however, ants were allowed to join the aphids, the reproduction rate of the green morph increased, and the green aphids now reproduced as fast as the red aphids. Thus, in the presence of ants, the proportion between green and red morphs was stable.

It is not clear how the ants improve the reproduction rate of the green aphids, but it saves the green morph from local extinction.

Winter

In the field, almost all colonies are mixed. It is understandable that no pure red colonies are to be found. No ant would be interested in such colony, which produces only low quality honeydew, so it would be lost. But why don’t green colonies exist? Why wouldn’t the ants remove the red aphids from a mixed colony by eating them, so that only high quality honeydew would be produced?

Apparently, the presence of red aphids is advantageous for some reason. That has to do with the winter period, the researchers suggest. At the end of the season, the aphids give birth to daughters and sons, which mate and produce fertilized eggs that can overwinter if the host plant survives. However, after flowering in autumn, mugwort dies off. The researchers hypothesize that red aphids may suppress flowering, so that the plant persists. They are now going to test that idea.

Need each other

It would mean that the ant needs both aphid morphs, the green one for high quality honeydew, the red one to maintain the colony to the next season. It would also mean that the two types of aphids need each other. The red morph cannot do without the green one, which attracts attending ants, and the green morph cannot do without the red one, which prevents the host plant from dying off in winter.

But as dependent the aphid morphs may be on each other, they cannot live together for a long time without the ant interfering.

Willy van Strien

Photo: aphid tending ant Lasius japonicus and two colour morphs of Macrosiphoniella yomogicola. ©Ryota Kawauchiya

Bronnen:
Watanabe, S., J. Yoshimura & E. Hasegawa, 2018. Ants improve the reproduction of inferior morphs to maintain a polymorphism in symbiont aphids. Scientific Reports 8: 2313. Doi: 10.1038/s41598-018-20159-w
Watanabe, S., T. Murakami, J. Yoshimura & E. Hasegawa, 2016. Color polymorphism in an aphid is maintained by attending ants. Science Advances 2: e1600606. Doi: 10.1126/sciadv.1600606