Category Archives: Zoology

Friday Fellow: Common Sea Angel

by Piter Kehoma Boll

Last week I presented a beautiful sea snail, the common sea butterfly, with wing-like parapodia that allows it to swim. The sea butterflies belong to a group of marine gastropods known as Pteropoda due to this foot modified into fins. There are two main groups of pteropods, Thecosomata, that have a shell, and Gymnosomata, that don’t have a shell. While the shelled ones are called sea butterflies, the naked ones are called sea angels or naked sea butterflies.

The most popular sea angel is Clione limacina, the common sea angel. Its body is mostly transparent and, like all pteropods, has two parapodia that look like wings which, together with its elongate and shell-less body makes it look like an angel indeed. Despite its angelic appearance, the common sea angel is a fearsome creature.

Despite the serene appearance, meeting this beautiful gastropod can be a frightening experience. Foto by Kevin Raskoff, Hidden Ocean 2005 Expedition: NOAA Office of Ocean Exploration.

Being a predator, the common sea angel is specialized in eating the common sea butterfly. Both species share the same environment in arctic waters and their association is known for centuries. The way that the common sea angel captures and eats the common sea butterfly is impressive and kind of scary.

A specimen, that was washed ashore, on a human hand for comparison. Photo by iNaturalist user nbenson.*

When the sea angel detects a sea butterfly nearby, it starts a pursue and everts six adhesive buccal cones from its mouth, forming a basket-like structure. This structure is used to capture the sea butterfly and, once the poor shelled snail is traped, the sea angel rotates the sea butterfly’s shell until its opening is directed to the predator’s mouth.

After that, the terror begins. The poor sea butterfly has withdrawn into its shell by this time, but the sea angel uses a group of chitinous hooks in its mouth to perforate the sea butterfly’s body and, helped by the radula, pulls the whole body of the prey from inside the shell, swallowing it entirely at once. It is likely a horrible death for the poor sea butterfly. After finishing swallowing one sea butterfly, the common sea angel can go after another one in about 2 minutes.

Drawing of a common sea angel feeding on a common sea butterfly. BC = buccal cones, HK = chitinous hooks, S = the shell of the sea butterfly. Extracted from Lalli (1970).

While the life cycle of the common sea butterfly is short, lasting only a year, that of the common sea angel is much longer. As a result, there are no adult sea butterflies to serve as food for the common sea angel from later autumn to early spring. For a long time it was thought that the common sea angel would spend this whole time without eating, and indeed it was found that it can survive long periods in starvation. However, analyses of the stomach content of the common sea angel revealed the presence of amphipods and eventually calanoid copepods, suggesting that it can rely on some alternative food sources in cases of extreme necessity. Their main food, however, is the common sea butterfly with no doubt. They start to feed on them when they are still larvae, always capturing and ingesting sea butterflies that have a size similar to theirs.

Will the common sea angel be able to survive on these other prey types if the populations of the common sea butterfly decline due to climate change? If find it unlikely and I hope we don’t need reach a point in which this becomes an option.

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References:

Böer M, Graeve M, Kattner G (2006) Exceptional long-term starvation ability and sites of lipid storage of the Arctic pteropod Clione limacina. Polar Biology 30:571–580. doi: 10.1007/s00300-006-0214-6

Conover RJ, Lalli CM (1972) Feeding and growth in Clione limacina (Phipps), a pteropod mollusc. Journal of Experimental Marine Biology and Ecology 9(3):279–302. doi: 10.1016/0022-0981(72)90038-X

Kallevik IHF (2013) Alternative prey choice in the pteropod Clione limacina (Gastropoda) studied by DNA-based methods. Master thesis in Biology, The Arctic University of Norway.

Lalli CM (1970) Structure and function of the buccal apparatus of Clione limacina (Phipps) with a review of feeding in gymnosomatous pteropods. Journal of Experimental Marine Biology and Ecology 4(2):101–118. doi: 10.1016/0022-0981(70)90018-3

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

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Friday Fellow: Common Sea Butterfly

by Piter Kehoma Boll

People love to name sea creatures by making analogies with things found on land. Today’s species is one more of this type, being the best known species of the so-called sea butterflies and, therefore, known as the common sea butterfly. It has nothing to do with butterflies, though, and its scientific name, Limacina helicina, is better to describe it.

The common sea butterfly is a mollusk, more precisely a gastropod, and, as it has a shell, it is a “snail”. It does not crawl through the floor as most snails though. With a spiral shell measuring only about 10 mm in diameter, it lives in the water column and is sometimes described as a planctonic species. It can swim by itself, though, because its fleshy foot is changed into two expansions called parapodia that act as two large fins. Its shell is mostly transparent and the soft parts are mainly purple, although the parapodia are almost transparent as well.

The common sea butterfly is truly a beautiful creature, isn’t it? Photo by Russ Hopcroft, University of Alaska, Fairbanks.

The habitat of the common sea butterfly includes the cold waters of the Arctic region, including the Arctic Ocean and neighboring areas of the Atlantic and Pacific oceans. In the Pacific, it can occur southward to Japan and the northern parts of the United States. Larger specimens tend to inhabit deeper waters, up to 150 m deep, while smaller ones live closer to the surface, up to 50 m down. Until very recently, the common sea butterfly was thought to inhabit Antarctic waters as well but molecular studies revealed that the populations around Antarctica belong to a different species, Limacina antarctica.

See how fast they can beat their wings.

The diet of the common sea butterfly includes several smaller planktonic creatures, especially small crustaceans, such as nauplii (larvae) of copepods, as well as dinoflagellates, ciliates and diatoms. Juveniles of their own species are also very common, sometines making up the second most common item in their diet. In order to capture food, they produce a spherical web of mucus that floats above them in the water. This web traps other organisms in the water column and is later sucked and eaten by the sea butterfly together with the entrapped creatures. This web is very difficult to observe during the day because of diffuse refraction but appears clearly at night. When disturbed by light, however, the common sea butterfly tends to quickly swallow its web and sink to escape from danger.

A commo sea butterfly with its spherical mucous web seen as an oval concentration of finer particles right above the snail. Extracted from Gilmer & Harbinson (1986).

The thin shell of the common sea butterfly consists of aragonite, which is highly soluble and sensitive to changes in temperature and acidification of the water. Studies have shown that the expected increase in ocean acidification due to human-induced climate changes will probably have a negative impact on populations of the common sea butterfly and related species. This is particularly worrisome regarding the common sea butterfly because it is the a key species in Arctic ecosystems, being an important food source for many marine animals, such as fish, whales, birds and even other mollusks.

The little snail will not give up the fight so easily, though. Studies have shown that the periostracum (the outer organic layer of the shell) can prevent the aragonite to dissolve and an physical trauma that breaks the periostracum, allowing the direct contact of the aragonite with the water, is necessary to cause dissolution. And even when this happens, the common sea butterfly can compensate by building new aragonite layers on the inner surface of the shell and it is able to extract aragonite from water for this purpose even when the levels in water are very low.

The common sea butterfly is small but it is also tough.

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References:

Corneau S, Alliouane S, Gattuso JP (2012) Effects of ocean acidification on overwintering juvenile Arctic pteropods Limacina helicina. Marine Ecology Progress Series 456:279–284. doi: 10.3354/meps09696

Comeau S, Jeffree R, Teyssié JL, Gattuso JP (2010) Response of the Arctic pteropod Limacina helicina to projected future environmental conditions. PLoS One 5(6):e11362. doi: 10.1371/journal.pone.0011362

Gilmer RW, Harbinson GR (1986) Morphology and field behavior of pteropod molluscs: feeding methods in the families Cavoliniidae, Limacinidae and Peraclididae (Gastropoda: Thecosomata). Marine Biology 91:47–57. doi: 10.1007/BF00397570

Gilmer RW, Harbinson GR (1991) Diet of Limacina helicina (Gastropoda: Thecosomata) in Arctic waters in midsummer. Marine Ecology Progress Series 77:125–134.

Lischka S, Büdenbender J, Boxhammer T, Riebesell U (2011) Impact of ocean acidification and elevated temperatures on early juveniles of the polar shelled pteropod Limacina helicina: mortality, shell degradation, and shell growth.  Biogeosciences 8:919–932. doi: 10.5194/bg-8-919-2011

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From headache to migraine: is Xenacoelomorpha a basal bilaterian clade or a group of weird deuterostomes?

by Piter Kehoma Boll

Seven years ago I discussed the phylogenetic position of Acoelomorpha and their close relative, Xenoturbella, which together form the clade Xenacoelomorpha. Being very simple bilaterian animals, lacking almost every major structure common to most other bilaterians, their exact position is usually considered to be basal inside Bilateria but the idea that they are deuterostomes was raised after some molecular studies grouped them with the clade Ambulacraria, which includes echinoderms and hemichordates.

Being deuterostomes would mean that Xenacoelomorpha suffered a huge simplification of their anatomy. Back in 2013, when I wrote the other article, this was causing a lot of controversy but, a time after that, new molecular studies confirmed the basal position of Xenacoelomorpha and it became kind of well accepted that they are, indeed, the basalmost clade in Bilateria.

A simplified version of the animal tree of life showing the uncertain position of Xenacoelomorpha. The position of Placozoa and Ctenophora is not very clear too.

But once a trouble, always a trouble.

By 2019, a new study that tried to anticipate effects of systematic errors during molecular phylogeny studies, such as long-branch attraction, concluded that the basal position of Xenacoelomorpha is an artifact and that, when one tries to minimize the errors, their position as sister-group of Ambulacraria becomes clear. However, their tree also suggests that Deuterostomia is not monophyletic, as Chordates appear as sister-group to Protostomia and Xenacoelomorpha+Ambulacraria is the basalmost group, i.e., the sister group of the rest of the Bilateria. However, the idea of Deuterostomia not being monophyletic is very unexpected.

As I mentioned in my old post, the main problem in Xenacoelomorpha appearing inside Deuterostomia is related to their oversimplification. They lack almost everything that any typical bilaterian has. What would have forced them to become that simple?

Xenoturbella japonica, a xenacoelomorph. Credits to Nakano et al. (2017).*

Another recent study suggested that, in the case of Xenoturbella at least, this may be the result of their soft-substrate burrowing habits. They compare Xenoturbella to nudibranchs, among which some species have similar lifestyles. One of these nudibranchs, Xenocratena, was actually discovered at about the same time as Xenoturbella living in the same environment. They have a paedomorphic (more simplified, “baby-like”) anatomy compared to other nudibranchs. However, it is not at all as simple as Xenoturbella.

The burrowing nudibranch Xenocratena suecica. Credits to Martynov et al. (2020).*

On the other hand, there is another genus of nudibranchs that is indeed oversimplified, Pseudovermis, and it lives burrowed in soft substrate as well. Molecular analyses revealed that Pseudovermis is not closely related to Xenocratena but to Cumanotus, another burrowing nudibranch, which suggests that this simplification occurred twice among nudibranchs.

Phylogenetic relationships among nudibranchs. See Pseudovermis and Cumanotus at about 2 o’clock and Xenocratena at about 7 o’clock. Credits to Martynov et al. (2020).*

This is not an evidence that Xenoturbella is a simplified deuterostome, but it is a good argument. But what about the simplifications of Acoelomorpha? I think that if Xenoturbella was not closely related to Acoelomorpha I would be more willing to accept this hypothesis. My heart leans toward the hypothesis of basal Xenacoelomorpha, though. However, as any cientist should do, I will accept Xenacoelomorpha as deuterostomes if enough evidence is presented.

Xenoturbella is always the main problem in this equation, The nervous system of Acoelomorpha, for example, although simplified, has kind of the basic pattern found in all bilaterians and could have evolved from the oral ring in a cnidarian-like ancestor according to some hypotheses. In Xenoturbella, though, the nervous system is much weirder, being formed by a simple network of difuse neurons below their skin. I guess addressing the organization of the nervous system in all these groups is a good topic for another post.

If there is one thing, in my opinion, that makes the position of Xenacoelomorpha within Deuterostomia somewhat convincing is the fact that many features of Deuterostomia seem to be more primitive inside Bilateria when compared to those in Protostomia, so the position of Xenacoelomorpha among Deuterostomia is more plausible than their position among Protostomia(although this is not even considered possible anymore) for sure. We tend to think that deuterostomes are more “derived” simply because humans are deuterostomes. But this discussion is also a subject for another post.

What do you think? Are you team basal or team deuterostome?

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You may also like:

Hagfish: another phylogenetic headache

Xenoturbella: a growing group of weirdoes

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References:

Cannon JT, Vellutini BC, Smith J, Ronquist F, Jonfelius U, Hejnol A (2016) Xenacoelomorpha is the sister group to Nephrozoa. Nature 530: 89–93. doi: 10.1038/nature16520

Jondelius U, Raikova OI, Martinez P (2019) Xenacoelomorpha, a Key Group to Understand Bilaterian Evolution: Morphological and Molecular Perspectives. In: Pontarotti P (ed) Evolution, Origin of Life, Concepts and Methods. Cham: Springer International Publishing, . pp. 287–315. doi: 10.1007/978-3-030-30363-1_14

Martynov A, Lundin K, Picton B, Fletcher K, Malmberg K, Korshunova T (2020) Multiple paedomorphic lineages of soft-substrate burrowing invertebrates: parallels in the origin of Xenocratena and Xenoturbella. PLoS ONE 15(1): e0227173. doi: 10.1371/journal.pone.0227173

Philippe H, Poustka AJ, Chiodin M, et al. (2019) Mitigating Anticipated Effects of Systematic Errors Supports Sister-Group Relationship between Xenacoelomorpha and Ambulacraria. Current Biology 29(11):1818–1826. doi: 10.1016/j.cub.2019.04.009

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

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Friday Fellow: Lignano’s Macrostomum

by Piter Kehoma Boll

It’s time to come back to the fascinating flatworms and today I decided to talk about one of the most studied species in this group even though it was only formally described 15 years ago. Its name is Macrostomum lignano, or the Lignano’s macrostomum.

Macrostomum lignano.Photo by Lukas Schärer,**

Measuring 1 to 2 mm in length, the Lignano’s macrostomum belongs to the order Macrostomida, one of the basalmost flatworm groups. Its body is elongate and transparent, there are two small eyes close to the anterior end, which has a small rostrum (“snout”). The mouth is a little behind the rostrum. The posterior end is broad, forming a tail plate with many adhesive organs arranged in a U-shape.

Basic morphology of the Lignano’s macrostomum. Credits to Lengerer et al. (2014).*

The Lignano’s macrostomum was first collected in marine samples in the city of Lignano on the Adriatic Sea coast in northern Italy in 1995 and soon revealed to be very suitable for laboratory cultures. The natural environment of this species includes the sand and other sediments near the shore. It avoids light and, when at rest, remains attached to the substrate by its tail plate. It feeds on small organism, especially diatoms, which it ingests using its cylindrical pharynx, similarly to how most flatworms eat.

Also like most flatworms, the Lignano’s macrostomum and other macrostomids have special stem cells called neoblasts that fill their body. All differentiated cells in the body come from neoblasts and are continuously replaced by them, since its differentiated cells cannot continue reproducing. Neoblasts also give the Lignano’s macrostomum an impressive regenerative ability like that of many other flatworms such as planarians.

Even before its formal description in 2005, the Lignano’s macrostomum had already been identified as a potentially new model organism. It can be easily cultured in laboratory in Petri dishes and fed with diatoms. Its body has about 25,000 cells, which is a number small enough to facilitate studies on development, regeneration, ageing and gene expression and that is exactly what has been done in the past decades.

The Lignano’s macrostomum is hermaphrodite. The body contains two testes and two ovaries. The male copulatory apparatus contains a stylet, a hardened penis-like copulatory organ. When two macrostomums mate, they touch their ventral surfaces in a yin yang fashion (just like the guys from last week) and exchange sperm. This behavior is easily observed in laboratory and led the Lignano’s macrostomum to become a model organism for the study of sexual selection as well. But wait! Sexual selection in a hermaphrodite organism? Yes! I discussed this topic some time ago here.

Macrostomum lignano, reciprocal mating behaviour
Two Lignano’s macrostomums mating in the yin yang position. Photo by Lukas Schärer.***

Sometimes, when two macrostomums meet, they don’t find their partner that attractive, so having their eggs fertilized by that guy is not of their interest from the female side. However, their male side is still as male as any other and they want to fertilize as many eggs as possible. As a result, if the partner is not good enough, they still want it as a female but not as a male. The other guys is not interesting in being a female only though, so copulation only occurs if both partners accept to receive each other sperm. “I let you fertilize my eggs if you let me fertilize yours.” So that’s what they do.

A pair of flatworms, Macrostomum lignano, mating. See how the white one, in the end, bends over itself and sucks the other guy’s sperm out of the female pore in order to get rid of it. Notice, however, in the last drawing, that the sperm cells are still attached to the female pore. It did not work. Image extracted from Schärer et al. (2004).

However, after they delivered the sperm into each other’s body, they separate and may never see each other again. So the female side evolved a strategy to select better sperm. When the “bad partner” moves away, a macrostomum that received low-quality sperm bends over itself, connects its pharynx to its female genital pore, and sucks the other guy’s sperm out before it has the chance to fertilize its eggs. A clever strategy, right? But remember: just as this guy is getting rid of the other guy’s sperm, the other guy may be doing the same with this guy’s sperm. So a strategy must evolve to prevent the female personality to discard the sperm. And that is exactly what happened! The sperm cells of the Lignano’s macrostomum have hard bristles pointing backward that, when the cells is pulled back, enter the tissues in the female copulatory apparatus and remain stuck. Trying to pull them out is just like trying to pull porcupine quills out of the skin.

Watch the behavior in video.

Now the male side recovered the advantage that the female side would have if the bristles were not there. But this is evolution, and its effect on hermaphrodites is like having two different personalities fighting each other in the same body.

Life is not easy anywhere.

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References and further reading:

Egger B, Ladurner P, Nimeth K, Gschwentner R, Rieger R (2006) The regeneration capacity of the flatworm Macrostomum lignano—on repeated regeneration, rejuvenation, and the minimal size needed for regeneration. Development Genes and Evolution 216:565–577. doi: 10.1007/s00427-006-0069-4

Ladurner P, Schärer L, Salvenmoser W, Rieger RM (2005) A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes: Macrostomum lignano, n. sp. (Rhabditophora, Macrostomorpha). Journal of Zoological Systematics and Evolutionary Research 43(2):114–126. doi: 10.1111/j.1439-0469.2005.00299.x

Lengerer B, Pjeta R, Wunderer J et al. (2014) Biological adhesion of the flatworm Macrostomum lignano relies on a duo-gland system and is mediated by a cell type-specific intermediate filament protein. Frontiers in Zoology 11:12. doi: 10.1186/1742-9994-11-12

Mouton S, Willems M, Braeckman BP, Egger B, Ladurner P, Schärer L, Borgonie G (2009) The free-living flatworm Macrostomum lignano: A new model organism for ageing research. Experimental Gerontology 44(4):243–249. doi: 10.1016/j.exger.2008.11.007

Pfister D, De Mulder K, Hartenstein V et al. (2008) Flatworm stem cells and the germ line: Developmental and evolutionary implications of macvasa expression in Macrostomum lignano. Developmental Biology 319(1):146–159. doi: 10.1016/j.ydbio.2008.02.045

Pfister D, De Mulder K, Philipp I et al. (2007) The exceptional stem cell system of Macrostomum lignano: Screening for gene expression and studying cell proliferation by hydroxyurea treatment and irradiation. Frontiers in Zoology 4:9. doi: 10.1186/1742-9994-4-9

Schärer L, Joss G, Sandner P (2004). Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck, Marine Biology 145 (2) doi: 10.1007/s00227-004-1314-x

Wasik K, Gurtowski J, Zhou X et al. (2015) Genome and transcriptome of the regeneration-competent flatworm, Macrostomum lignano. PNAS 112(40):12462–12467. doi: 10.1073/pnas.1516718112

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

**Creative Commons License This work is licensed under a Creative Commons Attribution-ShareAlike 3.0 Unported License.

***Creative Commons License This work is licensed under a Creative Commons Attribution 2.0 Generic License.

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Friday Fellow: Japanese Sea Firefly

by Piter Kehoma Boll

Japanese sea waters can emit a beautiful blue light at night, especially when disturbed. This phenomenon is caused by bioluminescent organism. One of the most famous species that produce light in the sea is the sea sparkle, a dinoflagellate. Here, however, the light is caused by a crustacean, the ostracod Vargula hilgendorfii, known in Japan as 海蛍 (umihotaru, literally “sea firefly”). Thus, the name sea firefly is commonly used to refer to the bioluminescent ostracods of the genus Vargula, most of which live along the North American Pacific coast and the Caribbbean, with Vargula hilgendorfii being the only species to occur in Japan.

Liquid light on a Japanese beach. Photo by Tdub Photo extracted from Kobi Lighting Studio.

As all ostracods, the Japanese firefly is a very small crustacean. Their body measure about 2–3 mm in length and have proportionally large eyes with about 0.2 mm in diameter. They live in the sandy substrate of shallow waters up to 5 m deep, being, therefore, benthonic, and have nocturnal habits.

A male Japanese sea firefly. The black spot is the eye. Extracted from Ogoh & Ohmiya (2005).

The areas where the Japanese sea firefly is found are marked by very strong currents. Since they have a very poor swimming ability, they are not very good to disperse to new areas but at least are able to swim well enough to avoid being carried far away by the currents. Nevertheless, the strong Japan Current seems to have slowly moved the species northward since the last ice age.

Female Japanese sea fireflies are slightly larger than males. When they copulate, they pair by touching their ventral sides while lying in opposite directions, kind of like a yin yang. Being an ovoviviparous species, the eggs remain inside the mother until they hatch, so that the female gives birth to live juveniles. Newborns are much smaller than adults, of course, but otherwise behave exactly like them, so that this species does not have a planktonic larval stage like most crustaceans.

Individual animals glowing on the sand. Photo by Tdub Photo extracted from Kobi Lighting Studio.

The diet of the Japanese sea firefly is composed mainly of debris of all sorts, including dead animals. One of the easiest ways to capture them is simply by placing dead fish as traps in the water at night and waiting for them to come.

When the Japanese sea firefly is disturbed or attacked, it releases a luminous blue cloud. This happens by the ejection of two compounds, the substrate luciferin and its enzyme, luciferase. Luciferase catalyzes the reaction of luciferin with molecular oxygen, which emits the characteristic blue light. There is a reflecting organ near the posterior end of the animal that seems to increase the power of the emitted light, which may improve their ability to escape from predators.

The natural mirror in the Japanese sea firefly’s body can enhance its light. Extracted from Abe et al. (2000).

Luciferase enzymes are of research interest especially as reporter genes. When scientists want to know whether a specific gene is being expressed in an organism, they can attach another gene right after it so that this gene will necessarily be expressed together with the gene of interest. The luciferase of the Japanese sea firefly, usually named Vargula luciferase, has been studied as a reporter gene in mammals. After creating the chain formed by the gene of interest + luciferase and inserting it into a cell, one can know whether the gene is being expressed by applying luciferin to the cells. If they glow blue this means that the gene is indeed being expressed.

As you can see, even a tiny sea creature can have a profound influence on scientific research.

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More Ostracods:

Friday Fellow: Sharp-Toothed Venus Seed Shrimp (on 22 June 2018)

Friday Fellow: Stonewort Seed Shrimp (on 19 July 2019)

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References and further reading:

Abe K, Ono T, Yamada K, Yamamura N, Ikuta K (2000) Multifunctions of the upper lip and a ventral reflecting organ in a bioluminescent ostracod Vargula hilgendorfii (Müller, 1890). Hydrobiologia 419: 73–82. doi: 10.1023/A:1003998327116

Abe K, Vannier J (1995) Functional morphology and significance of the circulatory system of Ostracoda, exemplified by Vargula hilgendorfii (Myodocopida). Marine Biology 124: 51–58. doi: 10.1007/BF00349146

Kobayashi K, Ohmiya Y, Shinohara D, Nabetani T, Niwa H (2001) Purification and properties of the luciferase from the marine ostracod Vargula hilgendorfii. Proceedings of the 11th International Symposium on Bioluminescence & Chemiluminescence: 87–90.

Maeda Y, Ueda H, Hara T, Kazami J, Kawano G, Suzuki E, Nagamune T (1996) Expression of a Bifunctional Chimeric Protein A-Vargula hilgendorfii Luciferase in Mammalian Cells. BioTechniques 20: 116–121. doi: 10.2144/96201rr01

Ogoh K, Ohmiya Y (2005) Biogeography of Luminous Marine Ostracod Driven Irreversibly by the Japan Current. Molecular Biology and Evolution 22(7): 1543–1545. doi: 10.1093/molbev/msi155

Thompson EM, Nagata S, Tsuji FI (1989) Cloning and expression of cDNA for the luciferase from the marine ostracod Vargula hilgendorfii. PNAS 86(17): 6567–6571. doi: 10.1073/pnas.86.17.6567

Thompson EM, Nagata S, Tsuji FI (1990) Vargula hilgendorfii luciferase: a secreted reporter enzyme for monitoring gene expression in mammalian cells. Gene 96(2): 257–262. doi: 10.1016/0378-1119(90)90261-O

Vannier J, Abe K (1993) Functional Morphology and Behavior of Vargula Hilgendor Fii (Ostracoda: Myodocopida) From Japan, and Discussion of Its Crustacean Ectoparasites: Preliminary Results From Video Recordings. Journal of Crustacean Biology 13(1): 51–76. doi: 10.1163/193724093X00444

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Friday Fellow: Grasshopper Nematode

by Piter Kehoma Boll

About one and a half year ago, I presented the long and thread-like wood cricket’s worm, a parasite that can control the behavior of the wood cricket and leaves its body once becoming an adult. The wood cricket’s worm belongs to the phylum Nematomorpha, commonly known as horsehair worms. They are closely related to phylum Nematoda, the roundworms. And just like horsehair worms, roundworms also love to infect crickets and grasshoppers.

One of those species is Mermis nigrescens, known as the grasshopper nematode. This worm can be found all over the world where grasshoppers exist, although they seem to be more common in Eurasia and the Americas.

An adult, gravid female. Photo by wikimedia user Beentree.**

Adults of the grasshopper nematode live in the soil and are very large for a nematode. Males measure about 5 cm in length and females can reach 20 cm, which is much larger than most nematodes that infect insects. They are, therefore, very similar to horsehair worms in appearance and behavior. The body has a smooth surface and a pale brown color, with females having a red spot on their head, the chromatopore, which functions like an eye.

After adults mate in spring or summer, males usually die but females remain in the soil through fall and winter and emerge in the following spring after a rainfall. They show a black stripe running along the body that is caused by thousands of eggs inside. They climb the nearby vegetation, up to 3 m above the ground, and lay their eggs, which measure about 0.5 mm in length, on it.

A female climbing the vegetation. Photo by Wikimedia user Notafly.**

In order to be able to climb the vegetation, female grasshopper nematodes show positive phototaxis, i.e., they are attracted by light sources, which is the opposite of what happens with most nematodes that have eyes. In fact the female’s eye, the chromatopore, is a single structure, like a single eye, and seems to have evolved independently from other nematode eyes. Its red color is caused by a hemoglobin, like the one that makes our blood red, but in this case it seems to function as a light receptor.

A closeup of the female eye and a transverse section through it. Extracted from Burr et al. (2000).*

When the eggs are ingested by an orthopteran insect (usually a grasshopper but sometimes a katydid), they hatch almost immediately. The young worm pierces the grasshopper’s gut and enters its hemocoel, the “blood cavity” of the body.

An adult around its dead host, a katydid. Photo by Wikimedia user Beentree.**

There, the worm develops by absorbing nutrients from the insect’s blood directly through its cuticle. This leads to serious depletion in the insect’s levels of blood sugar, especially trehalose (the insect storage sugar) and body proteins. After reaching 5 cm or more in size, they leave the insect, killing it in the process, and continue their development in the soil until reaching the adult stage and starting the cycle all over again.

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References:

Burr AHJ, Babinzski CPF, Ward AJ (1990) Components of phototaxis of the nematode Mermis nigrescens. Journal of Comparative Physiology A 167: 245–255. doi: 10.1007/BF00188117

Burr AHJ, Hunt P, Wagar DR, Dewilde S, Blaxter ML, Vanfleteren JR, Moens L (2000) A Hemoglobin with an Optical Function. Journal of Biological Chemistry 275: 4810–4815. doi: 10.1074/jbc.275.7.4810

Burr AHJ, Schiefke R, Bollerup G (1975) Properties of a hemoglobin from the chromatrope of the nematode Mermis nigrescens. Biochimica et Biophysica Acta (BBA) – Protein Structure 405(2): 401–411. doi: 10.1016/0005-2795(75)90105-1

Gordon R, Webster JM (1971) Mermis nigrescens: Physiological relationship with its host, the adult desert locust Schistocerca gregaria. Experimental Parasitology 29(1): 66–79. doi: 10.1016/0014-4894(71)90012-9

Rutherford TA, Webster JM (1974) Transcuticular Uptake of Glucose by the Entomophilic Nematode, Mermis nigrescens. Journal of Parasitology 60(5): 804–808. doi: 10.2307/3278905

Rutherford TA, Webster JM (1978) Some effects of Mermis nigrescens on the hemolymph of Schistocerca gregaria. Canadian Journal of Zoology 56(2): 339–347. doi: 10.1139/z78-046

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Friday Fellow: Reddish Cuckoo Wasp

by Piter Kehoma Boll

Besides the well-known internal and external parasites that feed on resources of the host, nature has other types of parasitism as well. One of those types is the so-called brood parasitism, in which an animal puts its eggs in the nest of another animal so that they will be raised by foster parents, usually from a different species. Cuckoos are certainly the most famous brood parasites, laying their eggs in the nests of other birds.

But brood parasites exist among other animal groups as well, including, of course, the diverse order Hymenoptera. Wasps of the family Chrysididae are known as cuckoo wasps because they put their eggs in the nests of other wasps. One species of this family is Hedychrum rutilans, which I decided to call the reddish cuckoo wasp.

A reddish cuckoo was in the Netherlands. Photo by iNaturalist user v_s_*.

Adults of this species measure up to 1 cm in length and have a kind of ant-shaped body. Its most striking feature, however, is its metalic color, which is typical of cuckoo wasps. In the reddish cuckoo wasp, the abdomen and the front part of the thorax have a reddish tinge, while the rest of the body is somewhat green.

Living in Europe and the northermost regions of Africa, the reddish cuckoo wasp is a lovely nectar drinker as an adult. However, as a larva, it is a parasitoid. Females put their eggs inside another insect so that the larva feeds on the host from inside. However, as I mentioned, cuckoo wasps are brood parasites, hence the name cuckoo wasp. Thus, they do not hunt other insects to serve as hosts for their larvae. Instead, they invade the nests of another species, the European beewolf, which I presented last week, and lay their eggs on the bees that the European beewolf has hunted for its own offspring.

Reddish cuckoo wasp in France. Photo by iNaturalist user butor*.

When the egg of the reddish cuckoo wasp hatches, the larva starts to feed on the paralyzed bees and can even feed on the growing larvae of the beewolf. But how can the female cuckoo wasp manage to invade the beewolf’s nest without being noticed?

The surface of insects is covered by cuticular hydrocarbons (CHCs), which have several functions. They protect the body from water and have many functions for chemical communication, both intra- and interspecifically. Parasitoids, for example, rely on CHC cues to find their hosts, and many species, especially social insects such as bees and ants, use CHCs to recognize individuals of their own colony and to detect any invader, incluing parasitoids and brood parasites. Thus, a beewolf could easily locate a cuckoo wasp sneaking into its nest but natural selection made the necessary changes. The amount of CHCs on the surface of cuckoo wasps is way below the normal levels found in most insects. As a result, their smell is so weak that it cannot be perceived in a nest that reeks of beewolf CHCs.

A specimen in Russia. Photo by Shamal Murza.*

One strategy that beewolfs seem to have developed to reduce the levels of parasitism by the reddish cuckoo wasp is increasing their activity in the evening, when the cuckoo wasp activity is reduced. During this time, it is easier for beewolves to enter their nests without being detected by cuckoo wasps. When a beewolf detects a cuckoo wasp close to its nests, it attacks it ferociously. However, once a cuckoo wasp enters the nest, the beewolf is unable to recognize it even if running right into it due to its inability to chemically detect the invader.

Both parties, of course, will always try to find new ways to succeed. Nature is, afterall, a neverending arms race.

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References:

Kroiss J, Schmitt T, Strohm E (2009) Low level of cuticular hydrocarbons in a parasitoid of a solitary digger wasp and its potential for concealment. Entomological Science 12:9–16. doi: 10.1111/j.1479-8298.2009.00300.x

Kroiss J, Strohm E, Vandenbem C, Vigneron J-P (2009) An epicuticular multilayer reflector generates the iridescent coloration in chrysidid wasps (Hymenoptera, Chrysididae). Naturwissenschaften 983–986. doi: 10.1007/s00114-009-0553-6

Strohm E, Laurien-Kehnen C, Boron S (2001) Escape from parasitism: spatial and temporal strategies of a sphecid wasp against a specialised cuckoo wasp. Oecologia 129:50–57. doi: 10.1007/s004420100702

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Friday Fellow: European Beewolf

by Piter Kehoma Boll

Among the species of the highly diverse insect order Hymenoptera, many are known to be parasites or parasitoids of a variety of animals and plants. Commonly known parasited species include spiders and caterpillars, but some hymenopterans parasitize other hymenopterans.

One of such species is Philanthus triangulum, known as the European beewolf. The name beewolf refers to the fact that this wasp species hunts bees, particularly the common honey bee Apis mellifera. This species occurs throughout Europe and Africa, having several subspecies.

A female European beewolf in Gran Canaria, Spain. Photo by Juan Emilio.**

The European beewolf has about the same length as its prey, the common honey bee, but its body has a more typical wasp look. The abdomen and the legs are predominantly yellow, while the head and the thorax are mainly black and brown. The yellow abdomen has black transversal stripes that are typical in many wasp species but their width can vary. Males are smaller than females and have a characteristic trident-shaped light mark between the eyes that is absent or very small in females.

A male in Andalucia, Spain. See the trident-shaped mark between the eyes. Photo by flickr user gailhampshire.*

In colder regions, where the winter is harsh, adult European beewolves emerge as adults in early summer. Both male and female adults feed on the nectar of several plants. Females create large and sometimes complex burrows in sandy soils in open sunny places. The burrows may have up to a meter in length and have between 3 and 34 short tunnels, the brood cells, at the end, each of which will be used to raise one larva. Once finishing the burrow, the female searches for honeybees to hunt. When attacking the bee, the beewolf stings it behind the front legs and paralyzes it, and then flies back to the nest carrying the paralyzed bee below her between her legs. Up to five honeybees can be provided for each larva and serve as their only food during their development.

A female with a paralyzed bee in England. Photo by Martin Cooper.*

Males tend to live near female burrows and use sex pheromones to attract them. Although they are territorial, they can sometimes tolerate other males nearby because the increased release of feromones increases the chances of them being detected by the females.

After the female has provided each egg with enough food, it closes the burrow and leaves. However, since the larvae will remain several months in that closed and humid environment, they can end up suffering from mold growth that can destroy themselves or their food. Females seem to have developed several strategies to reduce this problem. First, before laying the egg on the bee, the wasp licks most of the bee’s surface, applying a secretion from a postpharyngeal gland. Although this secretion has no antimycotic properties, it seems to delay water condensation on the bee’s surface, which also delays the development of fungi, and at the same time prevents water loss from the bee’s body, ensuring that the larvae will have the necessary amount of water to survive.

Carrying a bee into the burrow in England. Photo by Charlie Jackson.*

Female beewolves also live symbiotically with bacteria of the genus Streptomyces, which they cultivate in specialized glands in their antennae. They “secrete” the bacteria into the brood cells before leaving and later, when the larvae hatch, they collect the bacteria and apply them on the surface of a coccoon that they build to overwinter. These bacteria thus prevent fungi or other bacteria from growing on the coccoon, protecting the larvae from infections.

Nature never stops amusing us with its wonderful strategies so beautifully built by natural selection.

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References:

Herzner G, Schmitt T, Peschke K, Hilpert A, Strohm E (2007) Food Wrapping with the Postpharyngeal Gland Secretion by Females of the European beewolf Philanthus triangulum. Journal of Chemical Ecology 33:849–859. doi: 10.1007/s10886-007-9263-8

Herzner G, Strohm E (2008) Food wrapping by females of the European Beewolf, Philanthus triangulum, retards water loss of larval provisions. Physiological Entomology 33:101–109. doi: 10.1111/j.1365-3032.2007.00603.x

Kaltenpoth M, Goettler W, Dale C, Stubblefield JW, Herzner G, Roeser-Mueller K, Strohm Erhard (2006) ‘Candidatus Streptomyces philanthi’, an endosymbiotic streptomycete in the antennae of Philanthus digger wasps. International Journal of Systematic and Evolutionary Microbiology 56: 1403–1411. doi: 10.1099/ijs.0.64117-0

Wikipedia. European beewolf. Available at < https://en.wikipedia.org/wiki/European_beewolf >. Access on 20 February 2020.

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Friday Fellow: Asian Clam

by Piter Kehoma Boll

Since humans appeared on Earth and started to migrate, they carried other species with them to new localities. This made humans not the only species to become invasive and, in the past centuries, with human movement throughout the planet becoming more and more intense, invasive species became more and more common.

Among bivalvian mollusks, two very popular invasive species are the golden mussel and the zebra mussel, but they are not the only ones. There is one small bivalvian that is not that often a nuisance in human activities but is certainly a problem for native species, the so-called Asian clam, Corbicula fluminea.

An Asian clam in Hong Kong. Photo by Tommy Hui.*

The Asian clam is native from Eastern Asia where it lives burried in the sediment of rivers, prefering sandy sediments in oxygen-rich waters. Their small bivalvian shell measures up to 5 cm although most adult specimens are about 3 cm long. They have a brown to golden color, sometimes combined, but the colored layers sometimes flake off, causing white blotches.

The food of the Asian clam consists mainly of phytoplankton that it filters from the sediment. Human populations from Eastern Asia, such as the Chinese and Koreans, often use the Asian clam as a food source. During the 20th century, when many East Asian people migrated to other countries, the Asian clam was carried with them to be raised as food. As a result, this mollusk was introduced in North and South American river basins and started to spread quickly

The Asian clam is not as tolerant to environmental changes as other invasive bivalvians but its advantage is its rapid reproduction. Although there are both dioic and hermaphrodite lineages in this species, the invasive populations are all hermaphrodites. Fertilization occurs inside the body of the mother clam and the larvae develop inside, being released already as tiny shelled individuals.

The first records of this species in North America are from areas in the west coast of the United States in the 1920s. One century later the species is found throughout the whole country, having reached the east coast in less than four decades, and going north to Canada and south to Mexico and Central America.

Asian clam in Massachusetts, USA. Photo by iNaturalist user jfflyfisher.*

In South America, the species was introduced simultaneously in the La Plata River between Argentina and Uruguay and in the Jacuí river in southern Brazil in the 1970s. Currently, less than 50 years later, it is found as far north as Colombia as southward into Patagonia. The species was also introuced in Europe, Africa and Australia.

Shells collected in the La Plata River in Buenos Aires, Argentina. Photo by Diego Gutierrez Gregoric.*

The main impact caused by the invasion of the Asian clam is that it competes with native bivalvians, frequently leading to local extinctions, which is a major threat especially to many rare species that may disappear in a few decades. Although impacts on human activities are not that common, there are cases of large numbers of individuals clogging pipes and other structures.

A shell in Colombia. Credits to iNaturalist user gerardochs.*

Since there are fossil records of species of the genus Corbicula in North America, a hypothesis was raised suggesting that, instead of an invasion, the spread of the Asian clam in this continent is actually a recolonization following the last glaciation and that these individuals may be the result of small populations that remained hidden somewhere. However, it is very unlikely that the species would have remained hidden in very small populations for thousands of years to suddenly start to spread like hell in a few decades. Humans are to be blamed, as always.

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References:

Araujo R, Moreno D, Ramos MA (1993) The Asiatic clam Corbicula fluminea (Müller, 1774) (Bivalvia: Corbiculidae) in Europe. American Malacological Bulletin 10(1): 39–49.

Planeta Invertebrados. Corbícula. Available at < http://www.planetainvertebrados.com.br/index.asp?pagina=especies_ver&id_categoria=27&id_subcategoria=0&com=1&id=143 >. Access on 13 February 2020.

Sousa R, Antunes C, Guilhermino L (2008) Ecology of the invasive Asian clam Corbicula fluminea (Müller, 1774) in aquatic ecosystems: an overview. Annales de Limnologie 44(2): 85–94. doi: 10.1051/limn:2008017

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Friday Fellow: Aloe Mite

by Piter Kehoma Boll

Some months ago I introduced a tiny wasp that causes galls in eucalyptus trees. Now I am going to present another tiny creature, even smaller than that wasp, that causes a very abnormal type of gall in species of the genus Aloe.

Called Aceria aloinis and commonly known as the aloe mite, this microscopic arachnid can be a nightmare to aloe species and to those that cultive them. They are so tiny that they are barely seen with the naked eye. Their body is elongate and cylindrical, vermiform, like a microscopic sausage, and the adults have only four legs instead of the typical eight of most arachnids. This is the typical appearance of most mites of the family Eriophyidae, known as gall mites.

Two aloe mites. Extracted from Deinhart (2011).

Feeding on the epidermal cells of aloe plants, the aloe mite leads to a huge problem in its host. Its effect leads to an abnormal and ugly growth forming a shapeless gall that is adequately known as aloe cancer. This cancer often has a sponge-like appearance and sometimes, more than only strange growths from the leaves, stems and inflorescences, it can appear as a cluster of malformed leaves.

An ugly gall formed by the aloe mite. Photo by Colin Ralston.*

This malformation most likely has some negative effects on the plant’s fitness but the main concern is because it makes ornamental aloe species aesthetically unappealing. The most simple way to get rid of the aloe mite is to cut off the infected parts and burn them.

But how did they get to the plant in the first place? Well, eriophyid mites in general use the wind to be carried from one place to another and the aloe mite is no exception. So you may be able to cure your plant with an amputation but if there are other infected plants in the region, the mites may soon be back.

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References:

Deinhart N (2011) Tiny Monsters: Aceria alionis. Cactus and Succulent Journal 83(3): 120–122. doi: 10.2985/0007-9367-83.3.120

Villavicencio LE, Bethke JA, Dahlke B, Vander Mey B, Corkidi L (2014) Curative and preventive control of Aceria aloinis (Acari: Eriophyidae) in Southern California. Journal of Economic Entomology 107(6):2088-2094.

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Filed under Arachnids, Friday Fellow, Zoology