Category Archives: Behavior

Friday Fellow: Blue Paddled Mosquito

by Piter Kehoma Boll

A common tropical disease in forested areas of South America and Africa is the yellow fever. Affecting most primate species, the yellow fever is usually transmitted by the famous mosquito Aedes aegypti, which also transmits the dengue and zika fevers, all caused by viruses of the genus Flavivirus.

But in forested areas of South and Central America, other mosquito species can also transmit the yellow fever to humans and monkeys. One of these species is Sabethes cyaneus, which I decided to call the blue paddled mosquito. This species occur from Mexico to Argentina and Brazil and, different from most mosquitos, is diurnal.

A female about to have a bloody lunch on a human in Mexico. Photo by Carlos Alvarez N.*

Even if you don’t find mosquitos nice creatures most of the time, you will have to admit that the blue paddled mosquito is a beautiful animal. The body of the adult is dark and has metallic blue shade on the dorsum and the legs, being slightly greener on the dorsum and slightly purpler on the legs. More than that, the second pair of legs have a large tuft of hair that makes it look like a pair of paddles.

But what is the function of those paddles? The first guess would be that they are sexually selected and are likely important during courtship behavior. But females also have paddles and, if they were the result of sexual selection caused by females on males, they would likely be much larger on males, which is not the case.

Another female feeding on a human, this time in Paraguay. Photo by Joaquin Movia.*

Males perform, indeed, a complex courtship ritual in front of the females using their paddled legs. When females are prepared to mate, they perch vertically on a branch and wait for males to come and dance before them. Most of the males are rejected by a female and, when she finally chooses a male, she will compulate only with him. Males, on the other hand, copulate with many females. This increases even more the idea that the paddles must have some importance on female choice.

Male (left) and female (right). Image extracted from South & Arnqvist (2008).

This is not what was found, though. When the paddles of a male are reduced in size or removed completely, he still has the same chances of getting a female than intact males. On the other hand, a female whose paddles were removed rarely attracts any male. She remains perched on her branch waiting and waiting and no male will come to dance for her. The interest that male blue paddled mosquitos have for paddles is so strong that they even approach other perched males with large paddles.

The reason why this species exhibits strong male preference and weak female preference is still a mystery but is a nice reminder that our ideas on sexual selection are not as well-established as we might think.

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References:

Hancock RG, Foster WA, Lee WL (1990) Courtship behavior of the mosquito Sabethes cyaneus (Diptera: Culicidae). Journal of Insect Behavior 3(3): 401–416. doi: 10.1007/BF01052117

South SH, Arnqvist G (2008) Evidence of monandry in a mosquito (Sabethes cyaneus) with elaborate ornaments in both sexes. Journal of Insect Behavior 21: 451. doi: 10.1007/s10905-008-9137-0

South SH, Arnqvist G (2011) Male, but not female, preference for an ornament expressed in both sexes of the polygynous mosquito Sabethes cyaneus. Animal Behaviour 81(3): 645–651. doi: 10.1016/j.anbehav.2010.12.014

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*Creative Commons License This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.

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Friday Fellow: Chinese Banyan Wasp

by Piter Kehoma Boll

During the past three weeks, I presented a fig tree, the Chinese Banyan, a thrips that parasitizes it, the Cuban Laurel Thrips, and a mite that parasitizes the thrips, the Cuban-Laurel-Thrips Mite. However, I haven’t wrote yet about one of the most interesting creatures that interacts with a fig tree: its pollinator.

In the case of the Chinese Banyan, its pollinator is the fig wasp Eupristina verticillata, which I named the Chinese Banyan Wasp. As all fig wasps, this species is very small and completely adapted to live with figs. They cannot survive without the exact fig species with which they interact and the fig species cannot reproduce without that exact wasp. How does this works?

Let’s start our story with an adult female Chinese banyan wasp. The females are black and very small, measuring around 1 to 1.2 mm in length only. This female is flying around looking for a young fig which will serve as her nest and her grave.

This is what a female Chinese Banyan wasp loooks like. Photo by Forest & Kim Starr.*

A fig, in case you don’t know, is not a real fruit in the botanical sense. It is actually a special kind of inflorescence called a syconium that is basically a flower-filled sack. The inner walls of a fig have many tiny male and female flowers and the only way to get to them is through a tiny hole at the fig’s appex. And this hole is only open during the initial stages of the fig’s development.

Chinese Banyan figs in their early stage. You can see the hole marked by a darker “areola” around them. That is the place through which a female fig wasp enters the fig. Credits to Wikimedia user Vinayaraj.**

When the female Chinese Banyan fig wasps is flying around, she is looking for a fig that is at this exactly stage of development. Once she finds one, she crawls inside the fig through that tiny hole. She usually loses her wings while doing that because the passage is too narrow. She evens needs to use her especially adapted mandible to help her go through. Once inside the fig, she looks for the female flowers, which are located at the base of the fig, away from the entrance. The male flowers, located right at the entrance, are not mature yet. However, the female wasps arrived with pollen that she gathered elsewhere (you will learn about that soon). When she reaches the female flowers, she introduces her ovopositor (the long structure at the end of her abdomen that is used to lay eggs) inside the female flower and lays one egg inside the flower’s ovary. Her ovopositor needs to have the exact size to reach the ovary to lay the egg. If it is too short, she is unable to complete her task. And while she is moving from flower to flower to lay eggs, she ends up pollinating them. After she has finished, she dies still inside the fig.

The ovaries that received an egg start to grow into a gall (a “plant tumor”) by influence of the insect and serve as food and shelter for the larvae that hatch from the eggs. A larva grows, pupates and turns into an adult inside a single gall. When the wasps have finally reached their adult stage, they leave the gall in which they were born. This happens when the fig reached its mature stage.

Males are the first ones to emerge. They are even smaller than the females and have a yellow to light-brown color. They gnaw their way through the gall and, once outside it (but still inside the fig) they start to look desperately for female wasps to inseminate. They do that by tearing other galls apart and, when a female is found trapped inside, they inseminate her. After that, the males dig a hole through the fig to the outside and die soon after, never experienced the external world.

A male Chinese Banyan wasp (right) compared to a female. Photo by Forest & Kim Starr.*

Female wasps then leave their galls and move towards the hole opened by the male. While doing that, they move over the now mature male flowers and become covered in polen. After leaving the fig, they search for another fig that is in its early stage of development, restarting the cycle.

When a female leaves a mature fruit, she needs to find an immature one soon after that because she will die in a couple of days. In other words, the only way for this to work is if there are figs in the right stage all year around, and that is what happens. Differently from most plant species, which produce flowers in a specific time of the year, fig trees are always flowering. Well, not exactly. One individual fig tree produces figs only in a specific period of the year. All the figs of that tree ripen at the same time, i.e., a fig tree has an intra-individual synchrony of flower maturation. However, other trees of the same species have different moments to produce flowers, i.e., there is an inter-individual asynchrony of flower maturation. This assures that a wasp will always find a fig at the suitable maturation stage when there are enough fig trees around and also assures that a fig tree will not be fertilized by its own pollen.

As I mentioned when I presented the Chinese Banyan, this tree can only produce viable figs when the wasp is present, so that populations introduced outside of their native range will only reproduce if the waps is introduced as well. However, the wasp will be unable to survive if there are not enough fig trees to provide it with figs all year round. It is a delicate relationship between a tiny, fragile and short-lived insect and a huge, resistant and long-lived tree. And they need each other to survive.

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References:

Cook J, Rasplus J-Y (2003) Mutualists with attitude: coevolving fig wasps and figs. TRENDS in Ecology and Evolution 18(5): 241–248.

Kjellberg F, Jousselin E, Hossaert-McKey M, Rasplus J-Y (2005) Biology, Ecology, and Evolution of Fig-pollinating Wasps (Chalcidoidea, Agaonidae). In Raman A, Schaefer CW, Withers TM (Eds.) Biology, ecology and evolution of gall-inducing arthropods. v.2. New Hampshire, Science, p.539-572.

McPherson JR (2005) A Recent Expansion of its Queensland Range by Eupristina verticillata, Waterston (Hymenoptera, Agaonidae, Agaoninae), the Pollinator of Ficus microcarpa l.f. (Moraceae). Proceedings of the Linnean Society of New South Wales: 126: 197–201.

Weiblen DG (2002) How to be a fig wasp. Annual Review of Entomology 47: 299–330.

Wiebes JT (1992) Agaonidae (Hymenoptera, Chalcidoidea) and Ficus (Moraceae): fig waps and their figs, VIII (Eupristina s.l.). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen 95(1): 109–125.

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Tospovirus and thrips: an alliance that terrifies plants

by Piter Kehoma Boll

I recently presented a thrips in the Friday Fellow section, in that case a thrips that infects mostly fig trees. This group of insects, which make up the insect order Thysanoptera, is poorly known by the general public, but is certainly known by gardeners and farmers, as they can be a serious nuisance for many plant types.

We could imagine thrips as being kind of the mosquitoes of plants. They pierce the surface of plants and suck their juices just like mosquitoes do with vertebrates. And we all know that a mosquito bite may lead to much more than a small blood loss and local irritation of the skin. Many parasites use mosquitoes as vectors to travel from host to host, including protists such as Plasmodium falciparum, which causes malaria, and many types of virus, such as those of the genus Flavivirus, which cause the yellow, dengue and zika fevers.

A similar thing happens in the association of thrips with plants. A special genus of virus, called Tospovirus, infects many plant species and uses thrips as a vector. Inside the thrips bodies, the viruses reproduce after infecting the epithelial cells of the gut and, from there, travel via blood to the salivary glands and, when a thrips perforates a plant, the virus is injected in it. The cycle is basically the same used by Flavivirus in mosquitoes and ticks to infect vertebrates. Isn’t it amazing how a virus such as Tospovirus can infect both an animal and a plant? But what exactly is the disease caused by these viruses?

Basil leaf infected with the tomato spotted wilt virus. Photo by Scot Nelson.**

One of the most common Tospovirus is the so-called Tomato spotted wilt virus (TSWV), which is considered one of the most economically devastating plant viruses in the world. It can infect many crops, such as tomato, tobacco, bellpepper, peanut and basil. The symptoms vary from plant to plant, but usually include stunting, poorly developed fruits, commonly with ring spots on the surface, and necrosis of the leaves. It is transmitted to plants by thrips of the genus Frankliniella, mainly the western flower thrips Frankliniella occidentalis. Although the virus usually needs several hours to be able to reinfect a plant after infecting a thrips, in ideal conditions the time can e as short as five minutes.

The western flower thrips Frankliniella occidentalis. Photo by Dave Kirkeby.*

But why would a thrips feed on an obviously sick plant, all ugly and full of spots? They would certainly prefer a healthy plant, but that would prevent the virus to spread. As a result, the virus developed several strategies to attract the thrips. The TSWV is able to increase the amount of free aminoacids in infected plants, and these are essential nutrients for egg production in thrips. As a consequence, infected plants become more nutritious and attract more thrips. Feeding on infected plants, the thrips will certainly get infected and at the same time ingest more nutrients than non-infected thrips. Thus, a sick thrips actually has an increased fitness and usually lays more eggs. The plants would certainly get effing scared if they were able to have emotions.

The Soybean vein necrosis virus (SVNV) is another Tospovirus of economic concern. As it names suggests, it attacks mainly soy plants, and its main vector is the soybean thrips Neohydatothrips variabilis. Infected soybean thrips produce significantly more offspring than non-infected ones, although heavily infected individuals lay few viable eggs. How do thrips bypass this problem? It’s simple! Once they are infected, they stop feeding on infected plants and prefer non-infected ones, which increases their reproductive success by avoiding becoming heavily infected and at the same time they spread the virus further to non-infected plants. A nightmare for the plants once more.

Soybean thrips Hydatothrips variabilis. Photo by Even Dankowicz.***

A recent study investigated the relationship of another Tospovirus-thrips pair, this time of the iris yellow spot virus (IYSV), which commonly attacks garlic and onion plants, and its main vector, the onion thrips, Thrips tabaci. Infected thrips did not show an increased daily fecundity but had an increased lifespan, allowing them to lay more eggs simply because they lived longer.

Iris yellow spot virus lesion on an onion leaft. Extracted from https://vegetableguide.usu.edu/diseases/onion/iris-yellow-spot-virus

But the effect of Tospovirus on thrips can go further. For example, although plants infected by the TSWV release more aminoacids that attract and increase the fecundity of thrips, the infections still seems to have some deleterious effects on the insect. Infected males of Frankliniella occidentalis increase their consumption of food juices and increase the transmission of the virus. Females, on the other hand, seem to need nutrients that cannot be found in plants. As a result, they increase the consumption of eggs of the two-spotted spider mite Tetranychus urticae, with which they often coexist. Although primarily herbivorous as most thrips, the western flower thrips eventually feeds on mite eggs, and being infected by TSWV makes females become more eager to eat eggs. This is certainly not a strategy of the virus itself as the other ones, since a female that is feeding on mite eggs does not contribute for the virus’ reproductive success. Nevertheless, this is an interesting phenomenon that show us how the interactions in a trophic web can be dynamic, changing, for example, due to an uninentional side effect of a virus trying to survive.

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References:

Keough S, Han J, Shuman T, Wise K, Nachappa P (2016) Effects of Soybean Vein Necrosis Virus on Life History and Host Preference of Its Vector, Neohydatothrips variabilis , and Evaluation of Vector Status of Frankliniella tritici and Frankliniella fusca. Journal of Economic Entomology 109(5): 1979–1987. doi: 10.1093/jee/tow145

Leach A, Fuchs M, Harding R, Nault BA (2019) Iris Yellow Spot Virus Prolongs the Adult Lifespan of Its Primary Vector, Onion Thrips (Thrips tabaci) (Thysanoptera: Thripidae). Journal of Insect Science 19(3): 8. doi: 10.1093/jisesa/iez041

Shrestha A, Srinivasan R, Riley DG, Culbreath AK (2012) Direct and indirect effects of a thrips‐transmitted Tospovirus on the preference and fitness of its vector, Frankliniella fusca. Entomologia Experimentalis et Applicata 145(3): 260–271. doi: 10.1111/eea.12011

Stafford-Banks CA, Yang LH, McMunn MS, Ullman DE (2014) Virus infection alters the predatory behavior of an omnivorous vector. Oikos 123(11): 1384–1390. doi: 10.1111/oik.01148

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A chameleonic tree frog

by Piter Kehoma Boll

When we think of animals changing colors to adapt to the background, we readily think of chameleons, or maybe of some extremely rapid color switchers such as cephalopods like octopuses and cuttlefish. However, many other animals have this ability too.

One example are tree frogs of the family Rhacophoridae, especially of the genus Rhacophorus.

Recently, the phenomenon was recorded for the first time for the species Rhacophorus smaragdinus in northeastern India. The animal was of a vivid green color when found but, as soon as the researchers handled it, it turned into a dull brown color in a matter of seconds, only to slowly go back to green after left alone.

A disturbed female of Rhacophorus smaragdinus made itself brown and started to get green again after left undisturbed for some minutes. Credits to CK et al. (2019).*

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Reference:

CK D, Payra A, Tripathy B, Chandra K (2019) Observation on rapid physiological color change in Giant tree frog Rhacophorus smaragdinus (Blyth, 1852) from Namdapha Tiger Reserve, Arunachal Pradesh, India. Herpetozoa 32: 95–99. doi: 10.3897/herpetozoa.32.e36023

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One more species joins the Husband-Killers Club

by Piter Kehoma Boll

Leia em português

Sexual cannibalism is the act of eating a sexual partner right before, during or right after copulation. Despite being a considerably rare behavior, its occurrence is very popular among the general public.

When sexual cannibalism occurs, it usually consists of the female eating the male. Two popular cases are those of mantises and of spiders, especially the black widow. This phenomenon, at least among black widows, is much rarer than most people think.

Female mantis eating a yummy male. Photo by Oliver Koemmerling.*

Although sometimes sexual cannibalism occurs because one of the partners mistakes the other for food, in many species it is a evolutionary selected strategy that assures that the female will eat enough for the offspring to develop properly. It may look horrible from our human point of view, especially if we think from the perspective of the male, but we must remember that passing your genes to the next generation is the main purpose of most organisms and, if the male succeeded in fertilizing the female’s eggs, his life has served his purpose and he can die happily.

Sexual cannibalism is, of course, almost exclusively observed among predators, which is kind of obvious. And, as I said above, is commonly performed by the female. One group that is famous for its female-empowered species is the insect order Hymenoptera, which includes bees, ants, wasps, sawflies, among others. Since many hymenopterans have some degree of sociality, in which societies are composed almost exclusively of females, and males are generated only for the purpose of reproduction, it is curious that sexual cannibalism has never been recorded in this group… until now.

A recently published study examined the mating behavior of a small parasitoid wasp, Gonatopus chilensis. This species belongs to the family Dryinidae, of which all species lay their eggs on insects of the suborder Auchenorrhyncha, which includes cicadas, leaf hoppers, plant hoppers, among others. The larvae, after hatching from the egg, feed on the hosts. Adult females of dryinid wasps are also voracious predators and feed on the same species on which they fed as larvae.

Male of Gonatopus chilensis (left) inseminating a female (a), and female eating a male (b and c). Extracted from Virla & Espinosa (2019).*

After copulation, females of G. chilensis were often observed trying to capture the males in the same way they capture their prey. However, in only one occasion the female was successful in capturing the male and ate its gaster (the large round portion that forms most of the abdomen in wasps). Since only one instance of cannibalism was observed, it may be a rare phenomenon in this species, but since several attempts to capture the male were seen, it seems that eating the male is an interesting idea for the females.

This is the first known case of sexual cannibalism in hymenopterans and, therefore, an important record that increased the number of groups in which this behavior is known to occur.

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Badass females are unpopular among praying mantids

Male dragonflies are not as violent as thought

Having few females turns male tortoises into rapists

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Reference:

Virla EG, Espinosa MS (2019) Observations on the mating behavior of a dryinid and first record of sexual cannibalism in the hymenoptera. Acta Ethologica. doi: 10.1007/s10211-019-00315-9

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Caught in the act: Insect sex preserved in amber

by Piter Kehoma Boll

A recently published paper describes a new species of insect of the order Zoraptera from two specimens found in mid-cretaceous amber from northern Myanmar.

The preserved couple. They did not leave descendants but were eternized in science. Credits to Chen & Su (2019).*

But the most impressive thing about this new pre-historic species, named Zorotypus pusillus, is the fact that the fossil contains a male and a female that apparently died while they were mating. This is concluded because the two individuals are very close to each other and the male has an elongate structure coming out of his abdomen, which is probably the aedeagus or intromittent organ, a penis-like organ found in most zorapterans and used to deliver sperm into the female.

A detail of the posterior end of the male showing the aedeagus or intromittent organ. An anatomical reconstruction is shown to the right. Credits to Chen & Su (2019).*

The order Zoraptera contains a very small number of species, currently 44 extant ones and 14 fossils. They are very small, live in groups and look like tiny termites, although they are not closely related to them. Most extant species mate with the male introducing its aedeagus into the female to deliver sperm, but at least one species, Zorotypus impolitus, does not copulate. In this species, the male deposits microscopic spermatophores on the abdomen of the female.

The discovery of the preserved mating behavior in this species from the cretaceous period indicates that the mating behavior seen in most extant species was already used by species living 99 million years ago. The origin of zorapterans is not well known yet, but this and other fossil species indicate that they exist at least since the beginning of the cretaceous.

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Reference:

Chen X, Su G (2019) A new species of Zorotypus (Insecta, Zoraptera, Zorotypidae) and the earliest known suspicious mating behavior of Zorapterans from the mid-cretaceous amber of northern Myanmar. Journal of Zoological Systematics and Evolutionary Research. doi: 10.1111/jzs.12283

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Becoming a stepfather to get laid: the unusual alloparental care in a small carpenter bee

by Piter Kehoma Boll

Leia em português

Last month, I made some comments on alloparental care, i.e., the act of caring for an offspring that is not yours.

Most of the times, when parental care exists in a species, it is performed by the mother only. When there’s a helper, it is usually the father among vertebrates, or siblings among arthropods, especially social insects, such as bees and ants. Males taking care of the offspring in social insects is unlikely to occur in most species because the male usually dies soon after mating.

However, an uncommon situation was recently discovered in Ceratina nigrolabiata, a species of small carpenter bee from the Mediterranean region. In this species, the female is polyandrous, i.e., it mates with several males, so that not all her offspring has the same father.

This is not the unusual part, though. The strange thing is that males of this species do not die after mating and help the female take care of the offspring. While the female leaves the nest to look for food, the male remains and take care of the eggs and larvae, protecting them from natural enemies, such as ants. However, as I said above, females of this species mate with a lot of males, and genetic studies revealed that the male guarding the nest is the father of only about 10% of the offspring.

Parental care in the small carpenter beee Ceratina nigrolabiata:
(A) The female arrives at the nest. A male is flying nearby, looking for a “single lady”
(B) The female greets her helping male
(C) Sectioned nest showing three cells with larvae/eggs and food and a fourth cell being built; the female is to the left and the male to the right.
Credits to Mikát et al. (2019) (See references).

So why do males of Ceratina nigrolabiata take care of the children of another male? What the team who studied this system discovered is that the longer a male takes care of a nest, the larger is the number of offspring that has him as the father. In other words, it seems that helping a female increases the chances of a male to mate with that female, thus increasing the number of descendants he has. Nevertheless, males rarely remained for a long time in the same nest, usually moving to another nest every week or so, which does not increase the amount of his own offspring in the nest.

The team also experimentally removed females from the nests to observe how the males would behave in the absence of a female. What they found out is that males usually abandon the nest when this happens, not giving a damn to the poor babies. Thus, it is likely that this male alloparental care is actually a byproduct of mate guarding, i.e., the male is there to assure that he will have access to the female whenever she is willing to mate. He doesn’t actually care for the young.

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Reference:

Mikát M, Janošik L, Černá K, Matuošková E, Hadrava J, Bureš V, Straka J (2019) Polyandrous bee provides extended offspring care biparentally as an alternative to monandry based eusociality. PNAS 116(13): 6238-6243. doi: 10.1073/pnas.1810092116

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