 |
| Peruphasma schultei |
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| structure of dolichodial |
References
Dossey, A.T., Walse, S.S., Rocca, J.R. & Edison, A.S. (2006). Single-insect NMR: a new tool to probe chemical biodiversity. ACS Chemical Biology 1(8): 511-514.
Showing posts with label biochemistry. Show all posts
Showing posts with label biochemistry. Show all posts
Thursday, 19 November 2015
Stinky sticks
I keep black beauty stick-insects, Peruphasma schultei which hide, not by looking like vegetation but by being black, velvety (hence non-reflective) and nocturnal. However, although usually calm when handled, they do have active defences which I discovered recently when retrieving a large females that had escaped to climb the curtains. I felt something wet on my hand, and when I looked there was a milky, eye-wateringly acrid liquid. I knew that a lot of stick-insects can spray defensive chemicals but hadn't witnessed this one before. Fortunately a quick Google told me that this had been investigated by Dossey et al. (2006), who discovered a new defensive compound that they named 'peruphasmal' after the insect producing it.
Peruphasmal is an isomer of dolichodial, a compound in the iridoid group.
Iridoids are found in many plants (usualy in the form of glycosides) and may be active ingredients in those used medicinally. They are also likely to have a defensive function, protecting the plant against herbivores. Dolichodial and its isomers are found in plant essential oils, and as in this case, in the defensive sprays and secretions of some insects, possible being sequestered from food plants, or being produced by the insect's metabolism (they are intermediate compounds in the production of alkaloids for example). My P. schultei are fed on privet (Ligustrum sp.) which is in the family Oleaceae, one of those known to produce iridoids, so sequestration is plausible. The toxin in Ligustrum appears to be the glycoside syringin, known originally from lilacs, but now known to be a white, crystalline, bitter toxin in many plants including privet, hence its alternative name 'ligustrin'. So, this is a likely candidate for the source of the insect's defence. In plants, iridoids are usually bound to glucose, and peruphasmal is also sprayed along with glucose. Whatever the source - there is more research, but not much - it is an effective defence; my reaction was to put the insect down and wash off the secretion - a predator would have been sprayed in the face...
References
Dossey, A.T., Walse, S.S., Rocca, J.R. & Edison, A.S. (2006). Single-insect NMR: a new tool to probe chemical biodiversity. ACS Chemical Biology 1(8): 511-514.
References
Dossey, A.T., Walse, S.S., Rocca, J.R. & Edison, A.S. (2006). Single-insect NMR: a new tool to probe chemical biodiversity. ACS Chemical Biology 1(8): 511-514.
Friday, 25 January 2013
Beetles that keep their supercool
A few days ago, I wrote about antifreeze proteins in overwintering plants, during which I mentioned in passing that there is a similar system in some insects, and that I might write about that too. So, here goes...
One of the key concepts here is 'thermal hysteresis' (TH), the difference that antifreeze chemicals (usually proteins, but there are exceptions) create between the melting and freezing points, thus inhibiting ice formation and crystal growth. In fish this effect can reduce the freezing point by up to 1.5°C, and in plants the effect is weaker, but in insects, it is much stronger, reflecting the colder temperatures experienced on land than in water (plants don't show this, but are very differently organised both morphologically and biochemically). For example, despite being intolerant to freezing, the Spruce Budworm moth Choristoneura fumiferana (family Tortricidae) can survive to around –30 °C due to the presence of antifreeze proteins (e.g. Doucet et al. 2002, Qin et al. 2007). More impressively, the Alaskan beetle Upis ceramboides (family Tenebrionidae) survives conditions as cold as –60 °C using a non-protein TH chemical called xylomannan (Walters et al. 2009) which is a combination of sugars (sacchardies) and fatty acids (Ishiwata et al. 2011) in the cell membrane where it appears to function by suppressing the freezing of water molecules within cells. Interestingly, xylomannan was already known to be present in the red seaweed Nothogenia fastigiata, and research on this has shown it to have anti-viral effects by inhibiting replication, including types of herpes, influenza and (to a lesser extent) HIV, among others (Damonte et al. 1994).
The Alaskan-Canadian 'red flat bark beetle' Cucujus clavipes puniceus (family Cucujidae) is another that can survive extremely low temperatures (some individuals 'supercooling' to -100 °C in the lab!), in this case due to the more typical TH proteins and also losing 60-70% of its water content in winter (presumably reducing the among that has to be prevented from freezing) (Sformo et al. 2010, Carrasco et al. 2012).
I could go on - there are plenty of other examples even if some of the mechanisms and biochemistry are not fullt understood - but the point is that (1) there are processes here which require more study (anti-virals anyone!) and (2) wherever we look, life is more resilient than we imagine, with tardigrades and bacteria able to survive in space and much work being done on 'extremophiles' in places such as hot springs and hydrothermal vents as well as the frozen Arctic. Maybe time for a bet at Ladbrokes on life being found in the liquid interior of Europa...
References
Carrasco, M.A., Buechler, S.A., Arnold, R.J., Sformo, T., Barnes, B.M. & Duman, J.G. (2012). Investigating the deep supercooling ability of an Alaskan beetle, Cucujus clavipes puniceus, via high throughput proteomics. Journal of Proteomics 75(4):1220-1234.
Damonte. E., Neyts, J., Pujol, C.A., Snoeck, R., Andrei, G., Ikeda, S., Witvrouw, M., Reymen, D., Haines, H. & Matulewicz, M.C. (1994). Antiviral activity of a sulphated polysaccharide from the red seaweed Nothogenia fastigiata. Biochemical Pharmacology 47(12): 2187-2192.
Doucet, D., Tyshenko, M.G., Davies, P.L. & Walker, V.K. (2002). A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. European Journal of Biochemistry 269(1): 38-46.
Ishiwata, A., Sakurai. A., Nishimiya, Y., Tsuda, S. & Ito, Y. (2011). Synthetic study and structural analysis of the antifreeze agent xylomannan from Upis ceramboides. Journal of the American Chemical Society
133(48): 19524-19535.
Qin, W, Doucet, D., Tyshenko, M.G. & Walker, V.K. (2007). Transcription of antifreeze protein genes in Choristoneura fumiferana. Insect Molecular Biology 16(4): 423-434.
Sformo, T., Walters, K., Jeannet, K., Wowk, B., Fahy, G.M., Barnes, B.M. & Duman, J.G. (2010). Deep supercooling, vitrification and limited survival to -100 °C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. Journal of Experimental Biology 213(3): 502-509.
Walters, K.R., Serianni, A.S., Sformo, T., Barnes, B.M. & Duman, J.G. (2009). A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. Proceedings of the National Academy of Sciences of the USA 106(48): 20210–20215.
 |
| Winter conditions in southern England |
One of the key concepts here is 'thermal hysteresis' (TH), the difference that antifreeze chemicals (usually proteins, but there are exceptions) create between the melting and freezing points, thus inhibiting ice formation and crystal growth. In fish this effect can reduce the freezing point by up to 1.5°C, and in plants the effect is weaker, but in insects, it is much stronger, reflecting the colder temperatures experienced on land than in water (plants don't show this, but are very differently organised both morphologically and biochemically). For example, despite being intolerant to freezing, the Spruce Budworm moth Choristoneura fumiferana (family Tortricidae) can survive to around –30 °C due to the presence of antifreeze proteins (e.g. Doucet et al. 2002, Qin et al. 2007). More impressively, the Alaskan beetle Upis ceramboides (family Tenebrionidae) survives conditions as cold as –60 °C using a non-protein TH chemical called xylomannan (Walters et al. 2009) which is a combination of sugars (sacchardies) and fatty acids (Ishiwata et al. 2011) in the cell membrane where it appears to function by suppressing the freezing of water molecules within cells. Interestingly, xylomannan was already known to be present in the red seaweed Nothogenia fastigiata, and research on this has shown it to have anti-viral effects by inhibiting replication, including types of herpes, influenza and (to a lesser extent) HIV, among others (Damonte et al. 1994).
The Alaskan-Canadian 'red flat bark beetle' Cucujus clavipes puniceus (family Cucujidae) is another that can survive extremely low temperatures (some individuals 'supercooling' to -100 °C in the lab!), in this case due to the more typical TH proteins and also losing 60-70% of its water content in winter (presumably reducing the among that has to be prevented from freezing) (Sformo et al. 2010, Carrasco et al. 2012).
I could go on - there are plenty of other examples even if some of the mechanisms and biochemistry are not fullt understood - but the point is that (1) there are processes here which require more study (anti-virals anyone!) and (2) wherever we look, life is more resilient than we imagine, with tardigrades and bacteria able to survive in space and much work being done on 'extremophiles' in places such as hot springs and hydrothermal vents as well as the frozen Arctic. Maybe time for a bet at Ladbrokes on life being found in the liquid interior of Europa...
References
Carrasco, M.A., Buechler, S.A., Arnold, R.J., Sformo, T., Barnes, B.M. & Duman, J.G. (2012). Investigating the deep supercooling ability of an Alaskan beetle, Cucujus clavipes puniceus, via high throughput proteomics. Journal of Proteomics 75(4):1220-1234.
Damonte. E., Neyts, J., Pujol, C.A., Snoeck, R., Andrei, G., Ikeda, S., Witvrouw, M., Reymen, D., Haines, H. & Matulewicz, M.C. (1994). Antiviral activity of a sulphated polysaccharide from the red seaweed Nothogenia fastigiata. Biochemical Pharmacology 47(12): 2187-2192.
Doucet, D., Tyshenko, M.G., Davies, P.L. & Walker, V.K. (2002). A family of expressed antifreeze protein genes from the moth, Choristoneura fumiferana. European Journal of Biochemistry 269(1): 38-46.
Ishiwata, A., Sakurai. A., Nishimiya, Y., Tsuda, S. & Ito, Y. (2011). Synthetic study and structural analysis of the antifreeze agent xylomannan from Upis ceramboides. Journal of the American Chemical Society
133(48): 19524-19535.
Qin, W, Doucet, D., Tyshenko, M.G. & Walker, V.K. (2007). Transcription of antifreeze protein genes in Choristoneura fumiferana. Insect Molecular Biology 16(4): 423-434.
Sformo, T., Walters, K., Jeannet, K., Wowk, B., Fahy, G.M., Barnes, B.M. & Duman, J.G. (2010). Deep supercooling, vitrification and limited survival to -100 °C in the Alaskan beetle Cucujus clavipes puniceus (Coleoptera: Cucujidae) larvae. Journal of Experimental Biology 213(3): 502-509.
Walters, K.R., Serianni, A.S., Sformo, T., Barnes, B.M. & Duman, J.G. (2009). A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. Proceedings of the National Academy of Sciences of the USA 106(48): 20210–20215.
Sunday, 20 January 2013
Deadly crystals: keeping the ice at bay
Looking at our frozen-solid garden pond, I couldn't help notice how healthy the water plants looked - they might be encased in ice in sub-zero temperatures, but they clearly hadn't been destroyed (just think of the soggy green mush that's left if you freeze lettuce). This got me thinking - it isn't the temperature per se that causes damage, it's the formation of ice crystals in cells and tissues.
Many animals have antifreeze chemicals in their blood and tissues e.g. cold-water fish such as the largely Antarctic notothenioids and the unrelated Arctic cod (Boreogadus saida). These have various types of glycoproteins that bind to small ice crystals, preventing them from growing and/or recrystallising (and in some cases there are systems allowing resistance to the damage caused by ice crystal formation). The precise mechanisms of the various classes of antifreeze protein aren't fully understood, but research has continued (e.g. Wierzbicki et al. 2007), with the shapes and orientations of the proteins being clearly important (as in enzymes) with effects seen at the ice-water interface where ice has many different faces for potential binding. So, what's the situation in plants? In broad terms it's quite similar - many overwintering plants produce antifreeze proteins that work in a similar way to those of fish, but there are some differences.
The first of these relates to the concept of 'thermal hysteresis'. This is the difference that antifreeze proteins create between the melting and freezing points, thus inhibiting ice formation and crystal growth. In fish this effect can reduce the freezing point by up to 1.5°C, but in plants the effect is weaker. Insect antifreeze proteins, by the way, have a much stronger hysteresis effect and are not all proteins (e.g. Walters et al. 2009 who report one comprised of saccharides and fatty acids, found in an Alaskan beetle) - maybe something for a future post...
Secondly, their function appears to be more to do with inhibiting the recrystallization of ice rather than preventing its formation (Griffith & Yaish 2004). They also have a different evolutionary origin, mostly having developed from proteins involved in tackling pathogens - indeed, some retain antifungal properties. In hindsight, maybe this isn't so surprising as a protein that can bind to a pathogen might plausably have a straightforward evolutionary path to be able to bind to somthing else.
Lastly, unlike the equivalent proteins found in fish and insects, plant antifreeze proteins have multiple ice-binding points (Griffith & Yaish 2004), though it is unknown (as far as I am aware) whether this is directly adaptive or simply a left-over from its pathogen-fighting evolutionary history.
So, next time you see a healthy looking plant in wintry conditions, these are the sorts of biochemical shenanigans going on inside - and a subject where a bit of extra biophysical amd molecular research could yield genuine breakthroughs.
References
Griffith, M. & Yaish, M.W. (2004). Antifreeze proteins in overwintering plants: a tale of two activities. Trends in Plant Science 9(8): 399–405.
Walters, K.R., Serianni, A.S., Sformo, T., Barnes, B.M. & Duman, J.G. (2009). A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. Proceedings of the National Academy of Sciences of the USA 106(48): 20210–20215.
 |
| Water mint (Mentha aquatica) in our frozen pond. |
Many animals have antifreeze chemicals in their blood and tissues e.g. cold-water fish such as the largely Antarctic notothenioids and the unrelated Arctic cod (Boreogadus saida). These have various types of glycoproteins that bind to small ice crystals, preventing them from growing and/or recrystallising (and in some cases there are systems allowing resistance to the damage caused by ice crystal formation). The precise mechanisms of the various classes of antifreeze protein aren't fully understood, but research has continued (e.g. Wierzbicki et al. 2007), with the shapes and orientations of the proteins being clearly important (as in enzymes) with effects seen at the ice-water interface where ice has many different faces for potential binding. So, what's the situation in plants? In broad terms it's quite similar - many overwintering plants produce antifreeze proteins that work in a similar way to those of fish, but there are some differences.
The first of these relates to the concept of 'thermal hysteresis'. This is the difference that antifreeze proteins create between the melting and freezing points, thus inhibiting ice formation and crystal growth. In fish this effect can reduce the freezing point by up to 1.5°C, but in plants the effect is weaker. Insect antifreeze proteins, by the way, have a much stronger hysteresis effect and are not all proteins (e.g. Walters et al. 2009 who report one comprised of saccharides and fatty acids, found in an Alaskan beetle) - maybe something for a future post...
Secondly, their function appears to be more to do with inhibiting the recrystallization of ice rather than preventing its formation (Griffith & Yaish 2004). They also have a different evolutionary origin, mostly having developed from proteins involved in tackling pathogens - indeed, some retain antifungal properties. In hindsight, maybe this isn't so surprising as a protein that can bind to a pathogen might plausably have a straightforward evolutionary path to be able to bind to somthing else.
Lastly, unlike the equivalent proteins found in fish and insects, plant antifreeze proteins have multiple ice-binding points (Griffith & Yaish 2004), though it is unknown (as far as I am aware) whether this is directly adaptive or simply a left-over from its pathogen-fighting evolutionary history.
So, next time you see a healthy looking plant in wintry conditions, these are the sorts of biochemical shenanigans going on inside - and a subject where a bit of extra biophysical amd molecular research could yield genuine breakthroughs.
References
Griffith, M. & Yaish, M.W. (2004). Antifreeze proteins in overwintering plants: a tale of two activities. Trends in Plant Science 9(8): 399–405.
Walters, K.R., Serianni, A.S., Sformo, T., Barnes, B.M. & Duman, J.G. (2009). A nonprotein thermal hysteresis-producing xylomannan antifreeze in the freeze-tolerant Alaskan beetle Upis ceramboides. Proceedings of the National Academy of Sciences of the USA 106(48): 20210–20215.
Wierzbicki, A., Dalal, P., Cheatham, T.E., Knickelbein, J.E., Haymet, A.D.J. & Madura, J.D. (2007). Antifreeze proteins at the ice/water interface: three calculated discriminating properties for orientation of Type I proteins. Biophysical Journal 93(5): 1442–1451.
Thursday, 11 October 2012
Tarantula anatomy I: the abdomen
A few days ago, I was chatting with a friend of a friend on facebook after they posted a picture of the moulted skin of their pet Mexican Redknee Tarantula Brachypelma smithi. The upshot was that they offered to send me the skin so I could have a look at it under the microscope and see what interesting features were visible. It turns out that there were quite a lot - more than can fit into a single post - so here is part 1, looking at abdominal features.
The skin was well packaged and in really good condition and shows first of all how the spider moults. The top of the abdomen and cephalothorax split and peel back as a long flap, and the spider emerges up and backwards, pulling its legs and other appendages free. The new exoskeleton - including the fangs - is soft and needs to harden, and hence the spider will not be able to feed for a couple of days after moulting.
Looking at the abdomen, there are the familiar long bristles that you might expect to see, but a closer view (and indeed touch) shows that the texture is actually very different. There is a dense covering of shorter, softer hairs which look and feel much like moleskin - quite unexpected if you don't know what to expect!
The long bristles are important as they have a sensory function, whicle some others form an important defence mechanism, being brushed off towards potential predators using the legs. These 'urticating' hairs (the paler patch top left in the photo above) are much smaller but are barbed and cause irritation to areas such as the eyes. In the wild, the spider would spend most of its time in a burrow in an earth bank and use these hairs to deter predators such as coatis - though large and fearsome-looking, these spiders rarely bite and have only weak venom. In this genus, the urticating hairs are classified as Type III (there are six recognised types) which are 0.3–1.2 mm long and particularly irritating to mammals, including humans who sometimes develop a rash as an allergic reaction. The biochemistry of the hairs is poorly known - they appear to be chitnous and are certainly not made of living tissue - their irritating effects have been assumed to be physical (i.e. the effect of having barbed hairs stuck in your eyes/skin), but there may also be direct chemical effects, at least in some species.
The last feature I want to look at here are the book lungs, a series of flat membranes (lamellae) that spiders use for breathing via a pair of pores (spiracles) and which increase the surface area for gas exchange in much the same way as alveoli do in our lungs. They are named after their overall form which is similar to a stack of pages in a book. In this specimen, initially they were deflated and looked like quite unremarkable white masses, but when teased apart, some of the fine structure could be seen with the lamellae attached to branches leading to the spiracle and thus the outside air.
So, just a few abdominal features here - after all, the spider took its other organs with it! However, they are still interesting and there's more to come as I will be writing about the cephalothorax and appendages soon...
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| Dorsal view of the tarantula skin as it arrived in the post |
Looking at the abdomen, there are the familiar long bristles that you might expect to see, but a closer view (and indeed touch) shows that the texture is actually very different. There is a dense covering of shorter, softer hairs which look and feel much like moleskin - quite unexpected if you don't know what to expect!
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| The soft hairs of the abdomen along with longer, coarser bristles. |
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| The bases of two sensory bristles showing the attachment points that fit into 'sockets' in the exoskeleton. Mag x40 |
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| The fine hairs on the surface of a bristle. mag x100 |
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| Some of the small, defensive urticating hairs - note the thin attachment points and covering of barbs. Mag x40 |
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| Close-up of the barbs covering urticating hairs. Mag x100 |
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| A deflated book lung. |
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| Close-up of the book lung showing individual lamellae. |
Wednesday, 5 September 2012
Why Smurfs are like slipper limpets
Yes, I do mean Smurfs, those little blue Belgian cartoon characters... and slipper limpets are marine gastropods, Crepidula fornicata. So, why are they similar? Well, you probably know that, although there are lots of Smurfs (101 in fact), only one is female - Smurfette. Now, this could easily lead into pornographic territory (and undoubtedly has, somewhere on the Internet), but that's not what the Ecology Spot is about... instead I want to be a bit speculative and look at how this might affect Smurfs biologically if they were real...
One possibility would be that they became eusocial (like ants, bees and termites for example), with Smurfette as the only reproductive female (I assume Smurfs are viviparous, but maybe there are Smurf eggs - who knows?). However, Smurfette does not appear to be a large sedentary egg-layer (or large sedentary birther-of-live-young Smurflings), nor do there appear to be non-reproductive females rendered infertile by Smurfette pheromones. This is the case in, for example, the honey bee Apis mellifera, where the queen emits Queen Mandibular Pheromone (QMP), a pheromone set which, among other functions, inhibits ovary development in other females. So, the queen bee remains on the throne, and the princesses have to wait in line.With no other females present, and Smurfette running around actively, this seems unlikely. Instead, I think Smurfs might be an example of sequential hermaphroditism (SH).
One of the best-known examples of SH is C. fornicata. Though native to the eastern coast of North America, it has been widely introduced into the coastal waters of Europe, Japan and the NW Pacific, where it is invasive (having no predators away from its original range), competing with native filter-feeders for food. For more on its British history see here.
They can often be found in stacks and chains, their SH reproductive strategy meaning that the largest, oldest individuals, found at the base of the stack are female, while the younger, smaller ones at the top are male, and some in between are 'transient'. If the female(s) die, the largest male becomes a new female.
Proestou (2005) showed that C. fornicata tended towards a 1:1 sex ratio, and that as a male's distance from a female increased, his reproductive success decreased i.e. that the males closest to the female have a competitive advantage. From this, it follows that if these males suffer a reduction in reproductive success (e.g. from competition with other males) that is greater than that due toswitching sex at a small size, then they should change. Only the lowest male in a stack can change sex, a process that takes around 60 days, during which the penis regresses and the pouches and glands of the female duct develop. If a juvenile settles on an existing stack, it develops as a male and may stay like this for up to 6 years due to pheromones released by females at the base of the stack (Fretter & Graham, 1981). Presumably the death of a female means this pheromone ceases to be produced and thus the male can change sex - another process must prevent others from changing, possibly pheromones from the new female-to-be? As there are 'transients' which complicate the picture, a pheromone gradient seems plausible.
So, although the sex ratio is different in Smurfs (100:1 rather than 1:1), an SH strategy fits well. If Smurfette dies, then as the oldest male, Papa Smurf should become Mama Smurf, with some of the others (who after all, could be 'transient' and we wouldn't know by looking at them) waiting in line.
Next post - normal service will resume!
References
(1981). The Prosobranch Molluscs of Britain and Denmark. Part 6. Journal of Molluscan Studies Supplement 9: 309-313.
Proestou, D.A. (2005). Sex change in Crepidula fornicata: Influence of environmental factors on reproductive success and the timing of sex change. Dissertation, University of Rhode Island.
One possibility would be that they became eusocial (like ants, bees and termites for example), with Smurfette as the only reproductive female (I assume Smurfs are viviparous, but maybe there are Smurf eggs - who knows?). However, Smurfette does not appear to be a large sedentary egg-layer (or large sedentary birther-of-live-young Smurflings), nor do there appear to be non-reproductive females rendered infertile by Smurfette pheromones. This is the case in, for example, the honey bee Apis mellifera, where the queen emits Queen Mandibular Pheromone (QMP), a pheromone set which, among other functions, inhibits ovary development in other females. So, the queen bee remains on the throne, and the princesses have to wait in line.With no other females present, and Smurfette running around actively, this seems unlikely. Instead, I think Smurfs might be an example of sequential hermaphroditism (SH).
One of the best-known examples of SH is C. fornicata. Though native to the eastern coast of North America, it has been widely introduced into the coastal waters of Europe, Japan and the NW Pacific, where it is invasive (having no predators away from its original range), competing with native filter-feeders for food. For more on its British history see here.
 |
| A stack of C. fornicata (plus a small chiton on the left) - photo by F. Lamiot, and used here under the Creative Commons Attribution-Share Alike 1.0 Generic license. |
Proestou (2005) showed that C. fornicata tended towards a 1:1 sex ratio, and that as a male's distance from a female increased, his reproductive success decreased i.e. that the males closest to the female have a competitive advantage. From this, it follows that if these males suffer a reduction in reproductive success (e.g. from competition with other males) that is greater than that due toswitching sex at a small size, then they should change. Only the lowest male in a stack can change sex, a process that takes around 60 days, during which the penis regresses and the pouches and glands of the female duct develop. If a juvenile settles on an existing stack, it develops as a male and may stay like this for up to 6 years due to pheromones released by females at the base of the stack (Fretter & Graham, 1981). Presumably the death of a female means this pheromone ceases to be produced and thus the male can change sex - another process must prevent others from changing, possibly pheromones from the new female-to-be? As there are 'transients' which complicate the picture, a pheromone gradient seems plausible.
So, although the sex ratio is different in Smurfs (100:1 rather than 1:1), an SH strategy fits well. If Smurfette dies, then as the oldest male, Papa Smurf should become Mama Smurf, with some of the others (who after all, could be 'transient' and we wouldn't know by looking at them) waiting in line.
Next post - normal service will resume!
References
(1981). The Prosobranch Molluscs of Britain and Denmark. Part 6. Journal of Molluscan Studies Supplement 9: 309-313.
Proestou, D.A. (2005). Sex change in Crepidula fornicata: Influence of environmental factors on reproductive success and the timing of sex change. Dissertation, University of Rhode Island.
Monday, 13 August 2012
Fascinating toxic frogs
I'm moving away from my usual topic today by looking at a species that is neither British nor invertebrate - the green and black poison arrow frog Dendrobates auratus. Poison arrow/dart frogs (they have several non-scientific names) are familiar to many people because of their toxicity and bright colours, but what is actually known about them?
Well, first of all, although there are around 175 species of arrow/dart frogs (all in the family Dendrobatidae), only 3 are known to be used to coat blowpipe darts with poison, and none of these are in the genus Dendrobates. So, we know that the common name is not an accurate description - good start! Now onto a little background info.
Found in humid lowland and submontane forest and secondary vegetation up to about 1,200m altitude, D. auratus is native to Central America (Costa Rica, Nicaragua & Panama) and NW Colombia and, although many dendrobatids (like many amphibians worldwide) are rare and/or decreasing, this species is not currently threatened in the wild, being rated as of 'Least Concern' by the IUCN. There are also some feral populations in Oahu, Hawaii following a release of around 200 frogs in 1932 as an attempt to control non-native insects - these bred successfully and their descendents persist in the island's mountains and valleys (McKeown 1996). It is a highly variable species with at least 15 distinct colour forms known in the wild - as well as the typical green shown above, there is yellow, largely black, largely brown and the rare blue which is known from the Pacific side of Panama, but threatened with extinction due to clearance for agriculture, which fragments the habitat, though the species as a whole can live around humans (e.g. in parks, gardens and rubbish dumps (Heselhaus 1992, Ostrowski 2009). Being small (c. 20-40mm depending on form) and brightly coloured, tt is a popular pet among keepers of exotic herpetofauna and over-collection may be an issue, although there is a thriving captive breeding trade supplying much of the demand.
It is a semi-arboreal species, conducting much of its activity in trees up to some tens of metres above the ground but descending to the ground to travel between trees as it can not jump between them. Climbing is aided by pads at the ends of its toes (visible in the photo above). Females lay clutches of 3-13 eggs on leaf-litter which the male guards (Heselhaus 1992); they hatch after about two weeks and the male carries tadpoles to stagnant water in a tree-hole, leaf axil of a bromeliad, or small ground-level pool (van Wijngaarden 1990). The tadpoles feed on protozoans and rotifers, metamorphosing after 39-89 days, with sexual maturity being reached in 6-15 months, and a life-span of at least 6 years in captivity (Zimmermann & Zimmermann 1994). Females compete for males, attempting to monopolise them and being known to destroy the eggs of rivals (Summers 1989). If you would like to hear a brief recording of their call, go here.
Although not the most poisonous of dendrobatids, it is toxic enough to make a human unwell with skin glands producing an alkaloid derived from the ants that form much of the wild diet (Caldwell 1996). This reduces the risk of being attacked by predators such as theraphosid spiders AKA tarantulas (Gray et al. 2010), although some of the development of toxicity (e.g. in different popualtions, and captive-bred individuals fed a wild diet) are not fully understood.
So, to finish, why did I decide to look at this species? Well, it is a charismatic species and makes a change from my long run of invertebrate posts. I am also a member of Hampshire Conservation Volunteers - our logo is a frog so we adopted a D. auratus (now named 'Den Bates') at Marwell Wildlife and I wanted to know more about it - if you like this idea, the yellow and black D. leucomelas is still available for adoption...
References
Caldwell, J.P. (1996). The evolution of myrmecophagy and its correlates in poison frogs (Family Dendrobatidae). Journal of Zoology (London) 240(1): 75-101.
Gray, H.M., Kaiser, H. & Green, D.M. (2010). Does alkaloid sequestration protect the green poison frog,
Dendrobates auratus, from predator attacks? Salamandra 46(4): 235–238.
Heselhaus, R. (1992). Poison-arrow Frogs: Their Natural History and Care in Captivity. Blandford, London.
McKeown, S. (1996). A Field Guide to Reptiles and Amphibians in the Hawaiian Islands. Diamond Head Publishing, Los Osos, California.
Ostrowski, T. (2009). Dendrobates auratus. [accessed 13/08/2012].
Summers, K. (1989). Sexual selection and intra-female competition in the green poison-dart frog, Dendrobates auratus. Animal Behaviour 37(5): 797-805.
van Wijngaarden, R. (1990). Enkele klimaatgegevens en waarnemingen in de biotoop van de gifkikkers Phyllobates vittatus en Dendrobates auratus. Lacerta 48(5): 147-154.
Zimmermann, E. & Zimmermann, H. 1994. Reproductive strategies, breeding, and conservation of tropical frogs: dart-poison frogs and Malagasy poison frogs. In: J.B. Murphy, K. Adler and J.T. Collins (eds). Captive Management and Conservation of Amphibians and Reptiles. Society for the Study of Amphibians and Reptiles, Ithaca (New York). Contributions to Herpetology Volume 11, pp. 255-266.
 |
| Dendrobates auratus showing green and black colouration. |
Well, first of all, although there are around 175 species of arrow/dart frogs (all in the family Dendrobatidae), only 3 are known to be used to coat blowpipe darts with poison, and none of these are in the genus Dendrobates. So, we know that the common name is not an accurate description - good start! Now onto a little background info.
Found in humid lowland and submontane forest and secondary vegetation up to about 1,200m altitude, D. auratus is native to Central America (Costa Rica, Nicaragua & Panama) and NW Colombia and, although many dendrobatids (like many amphibians worldwide) are rare and/or decreasing, this species is not currently threatened in the wild, being rated as of 'Least Concern' by the IUCN. There are also some feral populations in Oahu, Hawaii following a release of around 200 frogs in 1932 as an attempt to control non-native insects - these bred successfully and their descendents persist in the island's mountains and valleys (McKeown 1996). It is a highly variable species with at least 15 distinct colour forms known in the wild - as well as the typical green shown above, there is yellow, largely black, largely brown and the rare blue which is known from the Pacific side of Panama, but threatened with extinction due to clearance for agriculture, which fragments the habitat, though the species as a whole can live around humans (e.g. in parks, gardens and rubbish dumps (Heselhaus 1992, Ostrowski 2009). Being small (c. 20-40mm depending on form) and brightly coloured, tt is a popular pet among keepers of exotic herpetofauna and over-collection may be an issue, although there is a thriving captive breeding trade supplying much of the demand.
It is a semi-arboreal species, conducting much of its activity in trees up to some tens of metres above the ground but descending to the ground to travel between trees as it can not jump between them. Climbing is aided by pads at the ends of its toes (visible in the photo above). Females lay clutches of 3-13 eggs on leaf-litter which the male guards (Heselhaus 1992); they hatch after about two weeks and the male carries tadpoles to stagnant water in a tree-hole, leaf axil of a bromeliad, or small ground-level pool (van Wijngaarden 1990). The tadpoles feed on protozoans and rotifers, metamorphosing after 39-89 days, with sexual maturity being reached in 6-15 months, and a life-span of at least 6 years in captivity (Zimmermann & Zimmermann 1994). Females compete for males, attempting to monopolise them and being known to destroy the eggs of rivals (Summers 1989). If you would like to hear a brief recording of their call, go here.
Although not the most poisonous of dendrobatids, it is toxic enough to make a human unwell with skin glands producing an alkaloid derived from the ants that form much of the wild diet (Caldwell 1996). This reduces the risk of being attacked by predators such as theraphosid spiders AKA tarantulas (Gray et al. 2010), although some of the development of toxicity (e.g. in different popualtions, and captive-bred individuals fed a wild diet) are not fully understood.
So, to finish, why did I decide to look at this species? Well, it is a charismatic species and makes a change from my long run of invertebrate posts. I am also a member of Hampshire Conservation Volunteers - our logo is a frog so we adopted a D. auratus (now named 'Den Bates') at Marwell Wildlife and I wanted to know more about it - if you like this idea, the yellow and black D. leucomelas is still available for adoption...
 |
| Mate-guarding in Dendrobates auratus |
References
Caldwell, J.P. (1996). The evolution of myrmecophagy and its correlates in poison frogs (Family Dendrobatidae). Journal of Zoology (London) 240(1): 75-101.
Gray, H.M., Kaiser, H. & Green, D.M. (2010). Does alkaloid sequestration protect the green poison frog,
Dendrobates auratus, from predator attacks? Salamandra 46(4): 235–238.
Heselhaus, R. (1992). Poison-arrow Frogs: Their Natural History and Care in Captivity. Blandford, London.
McKeown, S. (1996). A Field Guide to Reptiles and Amphibians in the Hawaiian Islands. Diamond Head Publishing, Los Osos, California.
Ostrowski, T. (2009). Dendrobates auratus. [accessed 13/08/2012].
Summers, K. (1989). Sexual selection and intra-female competition in the green poison-dart frog, Dendrobates auratus. Animal Behaviour 37(5): 797-805.
van Wijngaarden, R. (1990). Enkele klimaatgegevens en waarnemingen in de biotoop van de gifkikkers Phyllobates vittatus en Dendrobates auratus. Lacerta 48(5): 147-154.
Zimmermann, E. & Zimmermann, H. 1994. Reproductive strategies, breeding, and conservation of tropical frogs: dart-poison frogs and Malagasy poison frogs. In: J.B. Murphy, K. Adler and J.T. Collins (eds). Captive Management and Conservation of Amphibians and Reptiles. Society for the Study of Amphibians and Reptiles, Ithaca (New York). Contributions to Herpetology Volume 11, pp. 255-266.
Monday, 30 July 2012
Ants as farmers, aphids in the slow lane
If you grow soft fruit such as currants or gooseberries, you are probably familiar with the sight of numerous aphids densely clustered around the stems, making the leaves wrinkled and deformed. You may also be aware that some ant species 'farm' aphids in order to consume the sugar-rich 'honeydew' that they excrete. However, this is a complex behaviour and so is worth a closer look.
First of all, there are numerous aphid species that are found on cultivated fruits, and they can be difficult to tell apart. Those in the photo above are on black-currant Ribes nigrum - within the Ribes-feeding group, only one species has long, acute, erect to semi-erect hairs on the antennae (especially near the base), and that is what is seen here, Aphis schneideri (I couldn't get a clear photo of the antennal hairs, so you'll have to trust me on that). A. schneideri is also commonly associated with R. nigrum, causing clusters of terminal leaves to fold and distort, and the aphids are grey-green, with paler legs and often with a scattered coating of small pale waxy particles.
The ants seen attending the aphids here are the common black garden ant Lasius niger. Not all colonies of L. niger do this, although when it occurs, there is mutual benefit - the ants obtain sugar-rich honeydew and in turn protect the aphids from predators. So far, all straightforward, but exactly how the ants do this was not understood until a few years ago. It has been known for some time that, in order to ensure a dense crop of aphids, ants limit their dispersal (aphids otherwise disperse to new plants when overcrowded, the production of winged forms being triggered by the frequency of contacts between individuals) by biting off their wings (Kunkel 1973) or by secretions from the ants' mandibular glands interfering with the development of winged aphids (Kleinjan & Mittler 1975). Conversely, ants have been seen carrying aphids to suitable, good-quality host plants within their nest's home range. However, aphids also disperse by wandering (which may be more prevalent than dispersal by flying) and some decades ago, both Banks & Nixon (1958) and El Ziady (1960) noticed that the presence of ants seemed to slow aphids down, but no further research was undertaken until Oliver et al. (2007).
Ants are known to lay 'semiochemical' trails by touching glands onto the surface of their substrate, and these chemical marks can lead others from their nest sources of food (Hölldobler & Wilson 1990). Such chemicals can also be applied passively through shedding of cuticular hydrocarbons and this is important recognising nest-mates and, possibly, home-range territories (Devigne & Detrain 2002). Moreover, other insects, including herbivores and aphid predators, have been found to respond to chemicals that indicate the presence of ants (Offenberg 2004). However, Oliver et al. (2007) found that these ant chemicals had a tranquilising effect on aphids, causing them to walk more slowly and thus - as with the other effects noted above - maintain higher densities which provide the ants with more honeydew.
Although ants have been seen deterring aphid predators such as ladybirds, this does not mean that the mutualistic arrangement is entirely positive for the aphids. Their manipulation by ants means that their dispersal is reduced (or at least delayed) which may have impacts on the wider population (or 'metapopulation') and increase competition between closely packed individuals. Also, dense aggregations may be repeatedly attacked, and sometimes wiped out, by specialist parasitoids which are able to evade ants, such as the small parasitic wasp Lysiphlebus cardui (Weisser & Völkl 1997). Lastly, ants are occasionally seen eating aphids and it appears that this primarily occurs when individual aphids are encountered away from the aggregation. Not only would this prevent aphids being used for the benefit of rival neighbouring ant nests, but presumably produces an evolutionary pressure to 'obey' ant chemical cues rather than be able to avoid the tranquilising effect.
So, definitely a more complex story than it initially seemed (isn't it always!), but also a more interesting one, and something you may be able to witness in your own garden. If you are interested in identifying aphids, a standard work covering British Aphidini (the 'tribe' including the genus Aphis) is Stroyan (1984), but be warned - this is not an easy group to identify to species level, and the separation of some species can be uncertain.
References
Banks, C.J. & Nixon, H.L. (1958). Effects of the ant, Lasius niger L., on the feeding and excretion of the bean aphid, Aphis fabae Scop. Journal of Experimental Biology 35: 703-711.
Collins, C.M. & Leather, S.R. (200). Ant-mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality? Ecological Entomology 27: 238-241.
Devigne, C. & Detrain, C. (2002). Collective exploration and area marking in the ant Lasius niger. Insectes Sociaux 49: 357-362.
El Ziady, S. (1960). Further effects of Lasius niger L. on Aphis fabae Scopoli. Proceedings of the Royal Entomological Society A 35: 30-38.
Hölldobler, B. & Wilson, E.O. (1990). The Ants. Harvard University Press, Cambridge, MA.
Kleinjan, J.E. & Mittler, T.E. (1975). A chemical influence of ants in wing development in aphids. Entomologia Experimentalis et Applicata 18: 384-388.
Kunkel, H. (1973). Die Kotagabe der Aphiden (Aphidina, Hemiptera) unter Einfluss von Ameisen. Bonner Zoologische Beiträge 24: 105-121.
Offenberg, J. (2004). Evidence that insect herbivores are deterred by ant pheromones. Proceedings of the Royal Society B 271: S433-S435.
Oliver, T.H., Mashanova, A., Cook, J.M., Leather, S.R & Jansen, V.A.A. (2007). Ant semiochemicals limit apterous aphid dispersal. Proceedings of the Royal Society B: Biological Sciences 274: 3127-3131.
Stroyan, H.L.G. (1984). Aphids - Pterocommatinae and Aphidinae (Aphidini). Homoptera, Aphididae. Handbooks for the Identification of British Insects 2(6): 1-232.
Weisser, W.W. & Völkl, W. (1997). Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hym., Aphidiidae). Journal of Applied Entomology 121: 23-28.
 |
| A colony of Aphis schneideri on black-currant Ribes nigrum, attended by black garden ants Lasius niger |
The ants seen attending the aphids here are the common black garden ant Lasius niger. Not all colonies of L. niger do this, although when it occurs, there is mutual benefit - the ants obtain sugar-rich honeydew and in turn protect the aphids from predators. So far, all straightforward, but exactly how the ants do this was not understood until a few years ago. It has been known for some time that, in order to ensure a dense crop of aphids, ants limit their dispersal (aphids otherwise disperse to new plants when overcrowded, the production of winged forms being triggered by the frequency of contacts between individuals) by biting off their wings (Kunkel 1973) or by secretions from the ants' mandibular glands interfering with the development of winged aphids (Kleinjan & Mittler 1975). Conversely, ants have been seen carrying aphids to suitable, good-quality host plants within their nest's home range. However, aphids also disperse by wandering (which may be more prevalent than dispersal by flying) and some decades ago, both Banks & Nixon (1958) and El Ziady (1960) noticed that the presence of ants seemed to slow aphids down, but no further research was undertaken until Oliver et al. (2007).
Ants are known to lay 'semiochemical' trails by touching glands onto the surface of their substrate, and these chemical marks can lead others from their nest sources of food (Hölldobler & Wilson 1990). Such chemicals can also be applied passively through shedding of cuticular hydrocarbons and this is important recognising nest-mates and, possibly, home-range territories (Devigne & Detrain 2002). Moreover, other insects, including herbivores and aphid predators, have been found to respond to chemicals that indicate the presence of ants (Offenberg 2004). However, Oliver et al. (2007) found that these ant chemicals had a tranquilising effect on aphids, causing them to walk more slowly and thus - as with the other effects noted above - maintain higher densities which provide the ants with more honeydew.
Although ants have been seen deterring aphid predators such as ladybirds, this does not mean that the mutualistic arrangement is entirely positive for the aphids. Their manipulation by ants means that their dispersal is reduced (or at least delayed) which may have impacts on the wider population (or 'metapopulation') and increase competition between closely packed individuals. Also, dense aggregations may be repeatedly attacked, and sometimes wiped out, by specialist parasitoids which are able to evade ants, such as the small parasitic wasp Lysiphlebus cardui (Weisser & Völkl 1997). Lastly, ants are occasionally seen eating aphids and it appears that this primarily occurs when individual aphids are encountered away from the aggregation. Not only would this prevent aphids being used for the benefit of rival neighbouring ant nests, but presumably produces an evolutionary pressure to 'obey' ant chemical cues rather than be able to avoid the tranquilising effect.
 |
| A Lasius niger individual at a colony of Aphis schneideri |
So, definitely a more complex story than it initially seemed (isn't it always!), but also a more interesting one, and something you may be able to witness in your own garden. If you are interested in identifying aphids, a standard work covering British Aphidini (the 'tribe' including the genus Aphis) is Stroyan (1984), but be warned - this is not an easy group to identify to species level, and the separation of some species can be uncertain.
References
Banks, C.J. & Nixon, H.L. (1958). Effects of the ant, Lasius niger L., on the feeding and excretion of the bean aphid, Aphis fabae Scop. Journal of Experimental Biology 35: 703-711.
Collins, C.M. & Leather, S.R. (200). Ant-mediated dispersal of the black willow aphid Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality? Ecological Entomology 27: 238-241.
Devigne, C. & Detrain, C. (2002). Collective exploration and area marking in the ant Lasius niger. Insectes Sociaux 49: 357-362.
El Ziady, S. (1960). Further effects of Lasius niger L. on Aphis fabae Scopoli. Proceedings of the Royal Entomological Society A 35: 30-38.
Hölldobler, B. & Wilson, E.O. (1990). The Ants. Harvard University Press, Cambridge, MA.
Kleinjan, J.E. & Mittler, T.E. (1975). A chemical influence of ants in wing development in aphids. Entomologia Experimentalis et Applicata 18: 384-388.
Kunkel, H. (1973). Die Kotagabe der Aphiden (Aphidina, Hemiptera) unter Einfluss von Ameisen. Bonner Zoologische Beiträge 24: 105-121.
Offenberg, J. (2004). Evidence that insect herbivores are deterred by ant pheromones. Proceedings of the Royal Society B 271: S433-S435.
Oliver, T.H., Mashanova, A., Cook, J.M., Leather, S.R & Jansen, V.A.A. (2007). Ant semiochemicals limit apterous aphid dispersal. Proceedings of the Royal Society B: Biological Sciences 274: 3127-3131.
Stroyan, H.L.G. (1984). Aphids - Pterocommatinae and Aphidinae (Aphidini). Homoptera, Aphididae. Handbooks for the Identification of British Insects 2(6): 1-232.
Weisser, W.W. & Völkl, W. (1997). Dispersal in the aphid parasitoid, Lysiphlebus cardui (Marshall) (Hym., Aphidiidae). Journal of Applied Entomology 121: 23-28.
Friday, 27 July 2012
After the rains and beyond the pale...
...or 'from floods and the 2012 wildlife apocalypse to meadow creation via the wordy worlds of genetics and biochemistry'.
If you've been in the UK during the middle of 2012, you will have noticed that it's been raining a bit. Well, I say 'a bit', I actually mean a lot. Really a lot - following an unusually hot spring, it was wet from April to mid-July, including the wettest April for a century, and the wettest June on record. It's well understood that this was because the jet stream looped south of the UK and stayed there, but what is less well known is why this happened - this is an area of active research (including links to climate change) and there is an excellent summary here.
It has also been widely reported in both national and local media (e.g. here and here) that this unusually lengthy and heavy rainfall has had a huge impact on British wildlife - some species such as ringlet (Aphantopus hyperantus) butterflies (which breed in damp grassy areas) can do well in wet conditions, but current predictions are that 2012 will be the worst year on record for British butterflies overall. Volunteer recording will be hugely important in determining the effects on this group and there is still time to join in with the Big Butterfly Count which runs until 5th August. Although slugs and snails have done well (much to the annoyance of gardeners and vegetable growers), winged insects (including those most eseential of pollinators, bees) have fared poorly, being unable to feed or find mates effectively in cold, wet conditions and therefore are also unable to reproduce successfully. Although some mollusc-feeders may have plenty of food, this may well not lead to a good year for amphibians as the hot spring dried up breeding ponds and the April rainwater was too cold for reproduction. Thus, despite a few winners, the effect has largely been an overwhelmingly negative one e.g. many birds have been unable to keep chicks warm and fed, while many species, such as puffins, have seen nests flooded.
With widespread breeding failures, local extinctions have been predicted and conservationists are rightly worried about how severe the impacts will be, especially as the summer of 2011 was also poor. However, with the weather changing to become hot and sunny about a week ago, hopes for a good late summer and autumn have been fuelled, and I have to wonder to what extent various species can make up for lost time while conditions are suitable. Certainly my own observations, and those of other naturalists I've been in contact with, suggest that there is currently a rapid burst of invertebrate adult emergence, including species usually encountered earlier in the summer. Some moths which have emerged late have been reported as unusually pale, although this is from a fairly small number of observations, so its importance remains unclear. Delayed moth emergence related to temperature is well documented (e.g. DuRant 1990) but there does not appear to be any mention in the literature of aberrant colouration due to such delays. Certainly, a pale colour does not suggest an adaptive response as darker colours are generally associated with cooler temperatures as they permit more rapid warming by absorption of solar radiation. So, my question is whether delayed emergence can lead to paler colouration through some effect on the mechanisms related to pigmentation. Although this idea is somewhat speculative, two possibilities (which are not mutually exclusive) spring readily to mind:
1. Delayed emergence affects the mechanism of pigment production.
2. A longer period as a pupa means energy reserves become depleted and less essential material (such as pigments) is metabolised to enable emergence to be postponed during unfavourable conditions.
Looking at pigment production, some relevant research has been undertaken by Sawada et al. (2002) who looked at the expression of an mRNA-encoding guanosine triphosphate-cyclohydrolase I (GTP-CH I), the first key enzyme in the synthesis of pteridines during pigment formation in the wings of the butterfly Precis coenia. The biochemical details are not important here, but the key result was that gene expression was strongest one day before butterfly emergence. So, if pigment production is timed to peak around emergence, could a delay lead directly to reduced pigmentation? From this example, I have to say that it doesn't appear so - the onset and duration of gene expression appears to be controlled by the decline in the ecdysteroid hormone 20-hydroxyecdysone (linked to moulting and metamorphosis and usually called 20E), and a short delay in emergence simply led to a later peak in expression such that pigmentation and emergence remained synchronised. It is still possible that low temperatures prevent pigment formation though this implies the retention of higher levels of 20E and/or one of more effects elsewhere in the chain of biochemical processes involved. Essentially it seems that no-one knows if such effects occur.
Moving onto pigment breakdown, I'll stick with pteridines as there are a number of other pigment groups and I want to keep this at least reasonably simple. However, as Watt (1967) shows, the pteridine pathway is anything but simple, which in turn means that there are many points at which it might be disrupted, and as above, there is no indication that anyone has looked at the effects of delayed emergence on pigmentation, including the breakdown of pigment compounds.
So, although this has been a somewhat limited look at possible pigmentation effects, it has at least shown that it is an area where future research is needed. However, this does not mean that there is no every-day or real-world relevance here. Coming back to the 'volunteer' aspect mentioned earlier, it is not just recording that is needed, but habitat creation - in particular, the small-scale improvements that anyone with a garden can make (or indeed councils who own open spaces) by cultivating more-or-less natural 'meadow' areas rather than ecologically sterile mown lawns. Our garden is not large but it does include a meadow patch with scabious, bird's-foot trefoil, clovers, meadow clary, cornflower, lady's bedstraw, knapweeds and others. Not only is it more interesting and attractive than a billard-table lawn, but it has been a haven for flying insects throughout the wet summer - I have still identified around 25 bee species alone this year, with flowers being used during even the briefest of lulls in rainfall, and very actively during genuinely warm conditions. Also, you don't have to be an expert/experienced entomologist, botanist or gardener to do this. Wild flowers are in fashion at the moment (let's hope they stay that way rather than gravel, paving-for-parking and swathes of decking) with thoughtful gardening writers and TV presenters such as Sarah Raven promoting this important subject, including easy how-to guides if you want a garden meadow - and this means that garden centres and plant nurseries are likely to be well-stocked with native insect-friendly species. If you do this, not only will invertebrates reap the benefits, but so will you.
References
If you've been in the UK during the middle of 2012, you will have noticed that it's been raining a bit. Well, I say 'a bit', I actually mean a lot. Really a lot - following an unusually hot spring, it was wet from April to mid-July, including the wettest April for a century, and the wettest June on record. It's well understood that this was because the jet stream looped south of the UK and stayed there, but what is less well known is why this happened - this is an area of active research (including links to climate change) and there is an excellent summary here.
It has also been widely reported in both national and local media (e.g. here and here) that this unusually lengthy and heavy rainfall has had a huge impact on British wildlife - some species such as ringlet (Aphantopus hyperantus) butterflies (which breed in damp grassy areas) can do well in wet conditions, but current predictions are that 2012 will be the worst year on record for British butterflies overall. Volunteer recording will be hugely important in determining the effects on this group and there is still time to join in with the Big Butterfly Count which runs until 5th August. Although slugs and snails have done well (much to the annoyance of gardeners and vegetable growers), winged insects (including those most eseential of pollinators, bees) have fared poorly, being unable to feed or find mates effectively in cold, wet conditions and therefore are also unable to reproduce successfully. Although some mollusc-feeders may have plenty of food, this may well not lead to a good year for amphibians as the hot spring dried up breeding ponds and the April rainwater was too cold for reproduction. Thus, despite a few winners, the effect has largely been an overwhelmingly negative one e.g. many birds have been unable to keep chicks warm and fed, while many species, such as puffins, have seen nests flooded.
 |
| A pair of common garden snails Cornu aspersum (often known as Helix aspersa) |
With widespread breeding failures, local extinctions have been predicted and conservationists are rightly worried about how severe the impacts will be, especially as the summer of 2011 was also poor. However, with the weather changing to become hot and sunny about a week ago, hopes for a good late summer and autumn have been fuelled, and I have to wonder to what extent various species can make up for lost time while conditions are suitable. Certainly my own observations, and those of other naturalists I've been in contact with, suggest that there is currently a rapid burst of invertebrate adult emergence, including species usually encountered earlier in the summer. Some moths which have emerged late have been reported as unusually pale, although this is from a fairly small number of observations, so its importance remains unclear. Delayed moth emergence related to temperature is well documented (e.g. DuRant 1990) but there does not appear to be any mention in the literature of aberrant colouration due to such delays. Certainly, a pale colour does not suggest an adaptive response as darker colours are generally associated with cooler temperatures as they permit more rapid warming by absorption of solar radiation. So, my question is whether delayed emergence can lead to paler colouration through some effect on the mechanisms related to pigmentation. Although this idea is somewhat speculative, two possibilities (which are not mutually exclusive) spring readily to mind:
1. Delayed emergence affects the mechanism of pigment production.
2. A longer period as a pupa means energy reserves become depleted and less essential material (such as pigments) is metabolised to enable emergence to be postponed during unfavourable conditions.
Looking at pigment production, some relevant research has been undertaken by Sawada et al. (2002) who looked at the expression of an mRNA-encoding guanosine triphosphate-cyclohydrolase I (GTP-CH I), the first key enzyme in the synthesis of pteridines during pigment formation in the wings of the butterfly Precis coenia. The biochemical details are not important here, but the key result was that gene expression was strongest one day before butterfly emergence. So, if pigment production is timed to peak around emergence, could a delay lead directly to reduced pigmentation? From this example, I have to say that it doesn't appear so - the onset and duration of gene expression appears to be controlled by the decline in the ecdysteroid hormone 20-hydroxyecdysone (linked to moulting and metamorphosis and usually called 20E), and a short delay in emergence simply led to a later peak in expression such that pigmentation and emergence remained synchronised. It is still possible that low temperatures prevent pigment formation though this implies the retention of higher levels of 20E and/or one of more effects elsewhere in the chain of biochemical processes involved. Essentially it seems that no-one knows if such effects occur.
Moving onto pigment breakdown, I'll stick with pteridines as there are a number of other pigment groups and I want to keep this at least reasonably simple. However, as Watt (1967) shows, the pteridine pathway is anything but simple, which in turn means that there are many points at which it might be disrupted, and as above, there is no indication that anyone has looked at the effects of delayed emergence on pigmentation, including the breakdown of pigment compounds.
So, although this has been a somewhat limited look at possible pigmentation effects, it has at least shown that it is an area where future research is needed. However, this does not mean that there is no every-day or real-world relevance here. Coming back to the 'volunteer' aspect mentioned earlier, it is not just recording that is needed, but habitat creation - in particular, the small-scale improvements that anyone with a garden can make (or indeed councils who own open spaces) by cultivating more-or-less natural 'meadow' areas rather than ecologically sterile mown lawns. Our garden is not large but it does include a meadow patch with scabious, bird's-foot trefoil, clovers, meadow clary, cornflower, lady's bedstraw, knapweeds and others. Not only is it more interesting and attractive than a billard-table lawn, but it has been a haven for flying insects throughout the wet summer - I have still identified around 25 bee species alone this year, with flowers being used during even the briefest of lulls in rainfall, and very actively during genuinely warm conditions. Also, you don't have to be an expert/experienced entomologist, botanist or gardener to do this. Wild flowers are in fashion at the moment (let's hope they stay that way rather than gravel, paving-for-parking and swathes of decking) with thoughtful gardening writers and TV presenters such as Sarah Raven promoting this important subject, including easy how-to guides if you want a garden meadow - and this means that garden centres and plant nurseries are likely to be well-stocked with native insect-friendly species. If you do this, not only will invertebrates reap the benefits, but so will you.
 |
| The bee Andrena flavipes on white clover during the wettest summer on record. |
References
DuRant, J.A. (1990). Influence of temperature on spring emergence of European
corn borer moths (Lepidoptera: Pyralidae). Journal of Agricultural Entomology 7(3): 259-264.
Sawada, H., Nakagoshi, M., Reinhardt, R.K., Ziegler, I.& Koch, P.B. (2002). Hormonal control of GTP cyclohydrolase I gene
expression and enzyme activity during color pattern development in wings of Precis coenia. Insect Biochemistry and
Molecular Biology 32: 609–615.
Watt, W.B. (1967). Pteridine biosynthesis in the butterfly Colias eurytheme. Journal of Biological Chemistry 242(4): 565-562.
Thursday, 23 February 2012
Wheels of life
Straight in with a question today - have wheels evolved in nature? Now, I know it's been written about before, and there's no shortage of discussions on any number of online forums (or fora if you prefer), but it's something I've been musing on and coming up with some underlying questions - so, here goes with one my rare forays into the more speculative realms of biology and ecology...
Firstly, why might wheels be a useful adaptation? Well, they could provide an efficiency and simplicity of motion in some circumstances - I can certainly imagine animals using wide wheels to trundle across the soft sediments of the ocean floor for example (much like the wire-wheeled lunar rovers from Apollos 15-17). However, legs and fins generally work pretty well, with wheels really coming into their own on straight, smooth, hard surfaces. These are not common in nature, though humans produce plenty of them - and hence plenty of wheels. So, a lack of evolutionary advantage might be one reason why natural wheels are not widely seen.
Secondly, what do I even mean by a wheel? Here, I am only considering something that has an axle or bearing. There are plenty of organisms that roll - the South American pebble toad Oreophrynella nigra that tumbles down slopes to avoid predation, the wide variety of tumbleweed plants (and the rarer 'tumblefruits' such as Physaria) that disperse seeds as they roll with the wind, and the puffballs of the genus Bovista that are also blown around and so disperse their spores more widely. Ocean currents roll the coral Porites lutea across the sea floor and the small stomatopod mantis shrimp Nannosquilla decemspinosa can curl up and roll slowly like a wheel if stranded on a shallow damp sandy shore, thus returning to the sea. These are all interesting in their own right, and there are other examples, but none of them are wheels.
In fact, there don't appear to be any organisms that roll along on wheels in the way that humans' various vehicles do. As mentioned above, there may simply be no evolutionary pressure to produce a wheel, but there are also developmental constraints. For example, to have a wheel in a multicellular organism is tricky because, to be able to rotate freely, the wheel needs to be detached from the rest of the organism. If this is the case, how could it maintain a blood supply, neural connections and so on? Two options come to mind:
1. The wheel could be made of 'dead' material secreted by the organism, such as carapace material. This could grow as a toroid (doughnut-shaped) swelling on a limb/axle and gradually separate by thinning near the limb. This could produce a passive wheel on an axle much like a wood-turner produces a freely movable (but not removable) ring from a single piece of wood.
2. The wheel could be alive but self-contained. If a ring of cells developed as above and then detached, to be an effectively autonomous wheel, it would have to have its own energy supply (photosynthesis, chemosynthesis?) and so on.
Neither of these options have been discovered in nature, though this does not mean they never will - my feeling is that the lack of need is more likely to prevent wheels evolving than developmental problems. So far, I have not differentiated between passive and active wheels i.e. whether they simply roll like a cart (reducing the friction that would be caused by dragging) or are actively rotated by an energy source. Active wheels are developmentally even more problematic as a torque needs to be applied - in animals, motive force is produced by muscles, but this would not work on wheels as they need to be freely rotating. However, in bacteria, the problems of producing motive force, overcoming inertia and so on have been solved. In fact, the only example discovered so far of a true biological wheel (an active one that produces continuous propulsive torque around a fixed structure), is the bacterial flagellum, the a propeller-like thread used for locomotion. Where the flagellum enters the cell membrane, there is a motor protein that works like a rotary engine, powered the flow of hydrogen ions (i.e. protons) across the bacterial cell membrane down a concentration gradient created by a proton pump. A similar system using a sodium ion pump exists in the genus Vibrio.
At an even smaller scale, the enzyme ATP synthase (which is involved in energy storage and transfer within cells) is somewhat similar to bacterial flagellar motors and is likely to be an example of modular evolution i.e. where two separate structures or sub-units (which evolved and previously functioned separately) become joined or associated, and in doing so gain a new function.
So, although true wheels have not been discovered in multicellular organisms, and both developmental and utility constraints make their evolution highly unlikely, maybe impossible, there are ways that wheels might be used in nature:
1. Through symbiosis, joining two otherwise unrelated structures/organisms in order to get round the developmental problems preventing direct evolution of wheels. This could be instinctive (imagine an extension of dung-ball rolling by dung-beetles) and is an idea which has been explored in fiction, e.g. in the Amber Spyglass (Philip Pullman, 2000). In this book, an alien race known as the Mulefa use large, round seed pods as wheels. They put these on sideways-oriented claws (which act as axles) on two of their legs, using the other two legs to push themselves along. The symbiotic aspect occurs because the trees that produce the seed pods depend on the rolling action under the weight of the Mulefa to break open the pods and allow the seeds to disperse and germinate. A number of other science fiction novels consider biological wheel use in a variety of ways, but Pullman's is probably my favourite so far, though other examples include David Brin's Brightness Reef (1995) and Infinity's Shore (1996), and Wheelers (2000), co-authored by Ian Stewart and Jack Cohen (who happen to be a couple of Terry Pratchett's collaborators if you like a bit of nerd-trivia).
2. Through tool use. Humans do this, using wheels widely - could other species do the same, even if with less technological sophistication? I'm just waiting to see corvids start rolling past...
OK, I think that's enough speculation for one day - if anyone out there does know of other examples of 'bio-wheels', I love to hear about them, so feel free to add a comment.
Firstly, why might wheels be a useful adaptation? Well, they could provide an efficiency and simplicity of motion in some circumstances - I can certainly imagine animals using wide wheels to trundle across the soft sediments of the ocean floor for example (much like the wire-wheeled lunar rovers from Apollos 15-17). However, legs and fins generally work pretty well, with wheels really coming into their own on straight, smooth, hard surfaces. These are not common in nature, though humans produce plenty of them - and hence plenty of wheels. So, a lack of evolutionary advantage might be one reason why natural wheels are not widely seen.
Secondly, what do I even mean by a wheel? Here, I am only considering something that has an axle or bearing. There are plenty of organisms that roll - the South American pebble toad Oreophrynella nigra that tumbles down slopes to avoid predation, the wide variety of tumbleweed plants (and the rarer 'tumblefruits' such as Physaria) that disperse seeds as they roll with the wind, and the puffballs of the genus Bovista that are also blown around and so disperse their spores more widely. Ocean currents roll the coral Porites lutea across the sea floor and the small stomatopod mantis shrimp Nannosquilla decemspinosa can curl up and roll slowly like a wheel if stranded on a shallow damp sandy shore, thus returning to the sea. These are all interesting in their own right, and there are other examples, but none of them are wheels.
In fact, there don't appear to be any organisms that roll along on wheels in the way that humans' various vehicles do. As mentioned above, there may simply be no evolutionary pressure to produce a wheel, but there are also developmental constraints. For example, to have a wheel in a multicellular organism is tricky because, to be able to rotate freely, the wheel needs to be detached from the rest of the organism. If this is the case, how could it maintain a blood supply, neural connections and so on? Two options come to mind:
1. The wheel could be made of 'dead' material secreted by the organism, such as carapace material. This could grow as a toroid (doughnut-shaped) swelling on a limb/axle and gradually separate by thinning near the limb. This could produce a passive wheel on an axle much like a wood-turner produces a freely movable (but not removable) ring from a single piece of wood.
2. The wheel could be alive but self-contained. If a ring of cells developed as above and then detached, to be an effectively autonomous wheel, it would have to have its own energy supply (photosynthesis, chemosynthesis?) and so on.
Neither of these options have been discovered in nature, though this does not mean they never will - my feeling is that the lack of need is more likely to prevent wheels evolving than developmental problems. So far, I have not differentiated between passive and active wheels i.e. whether they simply roll like a cart (reducing the friction that would be caused by dragging) or are actively rotated by an energy source. Active wheels are developmentally even more problematic as a torque needs to be applied - in animals, motive force is produced by muscles, but this would not work on wheels as they need to be freely rotating. However, in bacteria, the problems of producing motive force, overcoming inertia and so on have been solved. In fact, the only example discovered so far of a true biological wheel (an active one that produces continuous propulsive torque around a fixed structure), is the bacterial flagellum, the a propeller-like thread used for locomotion. Where the flagellum enters the cell membrane, there is a motor protein that works like a rotary engine, powered the flow of hydrogen ions (i.e. protons) across the bacterial cell membrane down a concentration gradient created by a proton pump. A similar system using a sodium ion pump exists in the genus Vibrio.
 |
| The structure of the flagellar base showing cutaway details of the 'motor'. Thanks go to Mariana Ruiz Villarreal for putting this and other diagrams in the public domain. |
At an even smaller scale, the enzyme ATP synthase (which is involved in energy storage and transfer within cells) is somewhat similar to bacterial flagellar motors and is likely to be an example of modular evolution i.e. where two separate structures or sub-units (which evolved and previously functioned separately) become joined or associated, and in doing so gain a new function.
So, although true wheels have not been discovered in multicellular organisms, and both developmental and utility constraints make their evolution highly unlikely, maybe impossible, there are ways that wheels might be used in nature:
1. Through symbiosis, joining two otherwise unrelated structures/organisms in order to get round the developmental problems preventing direct evolution of wheels. This could be instinctive (imagine an extension of dung-ball rolling by dung-beetles) and is an idea which has been explored in fiction, e.g. in the Amber Spyglass (Philip Pullman, 2000). In this book, an alien race known as the Mulefa use large, round seed pods as wheels. They put these on sideways-oriented claws (which act as axles) on two of their legs, using the other two legs to push themselves along. The symbiotic aspect occurs because the trees that produce the seed pods depend on the rolling action under the weight of the Mulefa to break open the pods and allow the seeds to disperse and germinate. A number of other science fiction novels consider biological wheel use in a variety of ways, but Pullman's is probably my favourite so far, though other examples include David Brin's Brightness Reef (1995) and Infinity's Shore (1996), and Wheelers (2000), co-authored by Ian Stewart and Jack Cohen (who happen to be a couple of Terry Pratchett's collaborators if you like a bit of nerd-trivia).
2. Through tool use. Humans do this, using wheels widely - could other species do the same, even if with less technological sophistication? I'm just waiting to see corvids start rolling past...
OK, I think that's enough speculation for one day - if anyone out there does know of other examples of 'bio-wheels', I love to hear about them, so feel free to add a comment.
Wednesday, 15 February 2012
OMG in the OMZ: massive marine microbes
Today, I'm drawing inspiration from the Census of Marine Life, a decade-long project which has produced a huge inventory of marine life - a baseline catalogue to be used for further research and to inform the management and conservation of marine life. The Census looked at all scales from microbes to whales, at all latitudes and at all depths. The Census has produced a range of books, both popular and technical - one of the most straightforward and non-specialist, 'Citizens of the Sea' (Knowlton 2010) provided a couple of snippets that induced me to delve into the detail rather more...
First up, megabacteria - not the disease of budgies (which is actually a yeast), but very large true bacteria discovered off the coast of Chile and Peru in the 1960s. Placed in the genus Thioploca, the bacteria are filamentous and 2 to 7 cm (yes, cm) long. Secreting mucus, they form vast mats (the largest covering 130,000 km-sq) in/under the 'oxygen minimum zone' (OMZ), an area at 40-280 m with very little dissolved oxygen; instead they have to rely on hydrogen sulphide in the sediments. They oxidise this using nitrates (from sea water) which they can concentrate up to 500 mM in the liquid vacuole that occupies over 80% of their cell volume, even though the concentration of nitrates in sediment is only around 25 μM. Mucus-sheathed transport filaments send this nitrate 5–10 cm down into the sediment and reduce it, thus oxidising the hydrogen sulphide and creating a coupling of the nitrogen and sulphur cycles in the sediment (Fossing et al. 1994), producing pyrite and elemental sulphur as a result (Ferdelman et al. 1997). Thus, organic matter (in the form of anaerobic dissolved organic carbon) can be oxidised at low oxygen concentrations. The mats also provide food and shelter for a range of animals including squat lobsters (Pleuroncodes monodon), amphipods, and ophiuroids (Grupe 2011). As the OMZ shares features with conditions during the Proterozoic period (2.5 bya to 650 mya), and similar microfossils have been found, such bacteria may provide an insight into ancient life forms and ecology as well as performing a still little-known but key function in nutrient cycling. Research is ongoing with one recent example investigating Thioploca found in Danish waters where (in the species T. ingrica) nitrate accumulation was lower at around 3 mM, with bicarbonates and acetates used as carbon sources, and no mat being formed (Høgslund et al. 2010).
Now, ocean acidification due to carbon emission from fossil fuels may affect marine microbes - with microbial ecosystems responsible for between 50 and 90% of all marine biomass and over 95% of marine respiration, they maintain Earth's habitability though their influences on climate (they can sequester atmospheric carbon dioxide), nutrient cycling and the decomposition of pollutants (Leahy 2012). So, this could be very serious indeed and current research is looking at the sensitivity of marine microbes to acidification. If I find links to results from this research, I'll post an update, plus I have some more bacterial and marine posts (among others) in the pipeline.
References
Ferdelman, T.G., Lee, C., Pantoja, S., Harder, J., Bebout, B.M. & Fossing, H. (1997). Sulfate reduction and methanogenesis in a Thioploca-dominated sediment off the coast of Chile. Geochimica et Cosmochimica Acta 61(5): 3065-3079. Fossing, H, Gallardo, V.A., Jørgensen, B.B., Hüttel, M., Nielsen, L.P., Schulz, H., Canfield, D.E., Forster, S., Glud, R.N., Gundersen, J.K., Küver, J., Ramsing, N.B., Teske, A., Thamdrup, B. & Ulloa, O. (1994). Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca. Nature 374: 713-715.
Grupe, B. (2011). Sea Floor Habitats of the Chile Margin. NOAA Ocean Explorer [accessed 15/02/2012].
Høgslund, S., Nielsen, J.L. & Nielsen, L.P. (2010). Distribution, ecology and molecular identification of Thioploca from Danish brackish water sediments. FEMS Microbiology Ecology 73(1): 110-120.
Knowlton, N. (2010). Citizens of the Sea: Wondrous Creatures from the Census of Marine Life. National Geographic, Washington DC.
Leahy, S. (2012). Giant Bacteria Colonize the Oceans. Tierramérica. [accessed 15/02/2012].
First up, megabacteria - not the disease of budgies (which is actually a yeast), but very large true bacteria discovered off the coast of Chile and Peru in the 1960s. Placed in the genus Thioploca, the bacteria are filamentous and 2 to 7 cm (yes, cm) long. Secreting mucus, they form vast mats (the largest covering 130,000 km-sq) in/under the 'oxygen minimum zone' (OMZ), an area at 40-280 m with very little dissolved oxygen; instead they have to rely on hydrogen sulphide in the sediments. They oxidise this using nitrates (from sea water) which they can concentrate up to 500 mM in the liquid vacuole that occupies over 80% of their cell volume, even though the concentration of nitrates in sediment is only around 25 μM. Mucus-sheathed transport filaments send this nitrate 5–10 cm down into the sediment and reduce it, thus oxidising the hydrogen sulphide and creating a coupling of the nitrogen and sulphur cycles in the sediment (Fossing et al. 1994), producing pyrite and elemental sulphur as a result (Ferdelman et al. 1997). Thus, organic matter (in the form of anaerobic dissolved organic carbon) can be oxidised at low oxygen concentrations. The mats also provide food and shelter for a range of animals including squat lobsters (Pleuroncodes monodon), amphipods, and ophiuroids (Grupe 2011). As the OMZ shares features with conditions during the Proterozoic period (2.5 bya to 650 mya), and similar microfossils have been found, such bacteria may provide an insight into ancient life forms and ecology as well as performing a still little-known but key function in nutrient cycling. Research is ongoing with one recent example investigating Thioploca found in Danish waters where (in the species T. ingrica) nitrate accumulation was lower at around 3 mM, with bicarbonates and acetates used as carbon sources, and no mat being formed (Høgslund et al. 2010).
 |
| A core from a Thioploca bacterial mat. The core is about 8 cm across and the mat about 1 cm thick. The mat is made up of many bacterial filaments with individual cells visible to the naked eye as white threads. Huge for bacteria! Photo courtesy of NOAA/Lisa Levin. |
References
Ferdelman, T.G., Lee, C., Pantoja, S., Harder, J., Bebout, B.M. & Fossing, H. (1997). Sulfate reduction and methanogenesis in a Thioploca-dominated sediment off the coast of Chile. Geochimica et Cosmochimica Acta 61(5): 3065-3079. Fossing, H, Gallardo, V.A., Jørgensen, B.B., Hüttel, M., Nielsen, L.P., Schulz, H., Canfield, D.E., Forster, S., Glud, R.N., Gundersen, J.K., Küver, J., Ramsing, N.B., Teske, A., Thamdrup, B. & Ulloa, O. (1994). Concentration and transport of nitrate by the mat-forming sulphur bacterium Thioploca. Nature 374: 713-715.
Grupe, B. (2011). Sea Floor Habitats of the Chile Margin. NOAA Ocean Explorer [accessed 15/02/2012].
Høgslund, S., Nielsen, J.L. & Nielsen, L.P. (2010). Distribution, ecology and molecular identification of Thioploca from Danish brackish water sediments. FEMS Microbiology Ecology 73(1): 110-120.
Knowlton, N. (2010). Citizens of the Sea: Wondrous Creatures from the Census of Marine Life. National Geographic, Washington DC.
Leahy, S. (2012). Giant Bacteria Colonize the Oceans. Tierramérica. [accessed 15/02/2012].
Thursday, 9 February 2012
Antarctic sea spiders: polar or abyssal gigantism?
It is well known that in certain situations, some species evolve to be unusually large members of their taxonomic groups - the phenomenon of gigantism. Two such situations are polar and abyssal (deep-sea) gigantism, but why do large species evolve in polar and/or deep sea waters? As we will see, the answers are not always straighforward and are not necessarily the same for both situations. To illustrate this, I want to look at sea-spiders - not actually spiders but marine arthropods in the class Pycnogonida. A brief but informative introduction to this group can be found here, but in summary they are mostly free-living and are found at all latitudes and ocean depths. Superficially resembling spiders (though their taxonomic link to other groups is unclear), they have a cephalon (head) and a 4- (sometimes 5- or 6-) segmented body, each segment with a pair of walking legs (the rear segment bears a small abdomen), while the cephalon has various feeding appendages and palps, plus in males a pair of ovigers (leg-like appendages primarily used for carrying eggs & caring for young, but also for cleaning and courtship) which are found only in the Pycnogonida. Males also have 'cement glands' which they use to form eggs into round masses that are carried on the ovigers (Barnes 1980). Their biology is poorly studied - see Arnaud & Bamber (1987) for a useful review - but they reproduce by hatching as larvae or post-larvae with some being dispersed by medusae (jellyfish) and appear to feed on sessile animal prey or algae. Having such small bodies, their guts extend into their legs and in females, eggs are carried inside the femora. Around Britain, one common sea-spider is Pycnogonum littorale, a temperate shallow-water species (distribution given here) with a body around 5mm long and hence a leg-span of around 20mm.
In contrast, polar and/or deep-water species may have leg-spans up to 750mm, especially in the family Colossendeidae.
So, why this gigantism in polar and abyssal marine environments? As noted in the excellent Deep Sea News, it is unclear whether the cause is the same in both cases, and the two tend to be confused in scientific reporting by the media. Also, although giant sea-spiders are familiar examples of Antarctic gigantism, many are found in deep water and therefore a species may be subject to the processes of adaptation to both polar and abyssal conditions, making it difficult to separate the two effects. For example, specimens of C. wilsoni (photo above) in the Smithsonian Museum were found at depths between 36m and 801m, while the most common Antarctic species in this genus, C. megalonyx, has been found between 3m and 4,900m (Wu & Mastro 2004)! Hence, it is not clear whether gigantism in this species is polar or polar-and-abyssal.
A widely cited paper by Chapelle & Peck (1999), found that the maximum size of amphipods (shrimp-like crustaceans) was related to dissolved oxygen rather than temperature or salinity, with polar waters being high in dissolved oxygen, because water can hold more oxygen at low temperatures. Similar effects in bivalve molluscs have also been found (e.g. Pörtner et al. 2006). The reasoning behind this 'oxygen hypothesis' is that as the size of an organism increases, its surface area:volume ratio reduces. This means that larger animals have more tissue volume requiring oxygen, but relatively less surface area with which to sequester it from the surrounding water. In warmer waters, not only is their less dissolved oxygen, but the oxygen needs of animal tissues is higher. Thus polar gigantism occurs due to cold water temperatures and high levels of dissolved oxygen. However, more recent research involving the self-righting abilities of 12 different-sized species of sea-spider (Woods et al. 2008) did not fully support the oxygen hypothesis, although it did agree that oxygen availability was likely to be one important factor, just not the only one. A possible explanation is that, being an apparently early branch of sea-spider evolution (Arango & Wheeler 2007), Colossendeis species have been adapting to cold, well-oxygenated waters for a longer period that other genera and have oxygen delivery systems which are more finely tuned to such conditions. If this is the case, then climate change is a potentially serious threat to a specialist groups of species functioning with narrow oxygen safety margins i.e. warmer waters leading to higher oxygen demand and lower availability could push Colossendeis beyond these margins more quickly than it can adapt.
So, although it seems that polar gigantism is a result of oxygen availability plus other factors, abyssal gigantism is in some ways more mysterious. Firstly, as noted by Deep Sea News, much work has looked at deep sea dwarfism rather than gigantism because so many taxa show this reduction in size, suggesting that the deep ocean is primarily a small-organism habitat (McClain et al. 2005, Kaariainen & Bett 2010). Thus, the incidence of abyssal gigantism (seen particularly in crustaceans, but also a range of other taxa) contrasts strongly with what appears to be the 'normal' situation in the deep ocean.
Abyssal dwarfism has generally been attributed to low food availability, with most animal communities (away from seeps and vents) relying on the 'marine snow' of detritus sinking from the surface, with occasional larger localised inputs such as dead whales. Thus little food arrives, especially away from productive shallow coastal waters. However, several possible explanations for the rarer gigantism have been proposed e.g.:
However, although key effects such as the link between oxygen levels and cell size/number have been described, these are the result of work on unrelated taxa and it remains unclear precisely why Colossendeis sea-spiders (let alone giant isopods) should exhibit gigantism while others do not - and so it is tie for a little (hopefully not too idle) speculation:
Further reading
For a key to coastal British species: King, P.E. (1986). Sea Spiders. A revised key to the adults of littoral Pycnogonida in the British Isles. Field Studies 6(3): 493-516.
References
Arango, C.P. & Wheeler, W.C. (2007). Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23: 255–293. Arnaud, F. & Bamber, R.N. (1987). The Biology of Pycnogonida. Advances in Marine Biology 24: 1-96.
Bamber, R.N. & El Nagar, A. (eds.) (2012). Pycnobase: World Pycnogonida Database. [accessed 09/02/2012]
Barnes, R.D. (1980). Invertebrate Zoology (4th ed.). Holt-Saunders, Philadelphia.
Chapelle, G., & Peck L.S. (1999). Polar gigantism dictated by oxygen availability. Nature 399: 114-115.
Fisher, C.R., Urcuyo, I.A., Simpkins, M.A. & Nix, E. (1997). Life in the slow lane: growth and longevity of cold-seep vestimentiferans. Marine Ecology 18(1): 83-94.Frazier, M. R., Woods, H. A. & Harrison, J. F. (2001). Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiological and Biochemical Zoology 74: 641-650.
Kaariainen, J. & Bett, B. (2010). Evidence for benthic body size miniaturization in the deep sea. Journal of the Marine Biological Association of the UK. 86(6): 1339-1345.
Lomolino, M.V. (2005). Body size evolution in insular vertebrates: generality of the island rule. Journal of Biogeography 32(10): 1683-1699.
McClain, C.R & Rex, M.A. (2001). The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression. Marine Biology 139: 681-685.
(2005). Deconstructing bathymetric body size patterns in deep-sea gastropods. Marine Ecology Progress Series 297: 181-187.
Peck, L.S. & Chapelle, G. (2003). Reduced oxygen at high altitude limits maximum size. Proceedings of the Royal Society of London B (Suppl.) 270: S166-167.
Pörtner, H.O., Peck, L.S. & Hirse, T. (2006). Hyperoxia alleviates thermal stress in the Antarctic bivalve, Laternula elliptica: evidence for oxygen limited thermal tolerance. Polar Biology 29: 688-693.
gigantism not supported by performance of Antarctic pycnogonids in hypoxia. Proceedings of the Royal Society B 276: 1069-1075.
Wu, N. & Mastro, J. (2004). Under Antarctic Ice. University of California, Berkeley CA.
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| A display of Pycnogonum littorale at the OUMNH |
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| Colossendeis wilsoni, A large Antarctic sea-spider also in the OUMNH collection. For scale, the label font is the same size as in the photo of P. littorale above. |
A widely cited paper by Chapelle & Peck (1999), found that the maximum size of amphipods (shrimp-like crustaceans) was related to dissolved oxygen rather than temperature or salinity, with polar waters being high in dissolved oxygen, because water can hold more oxygen at low temperatures. Similar effects in bivalve molluscs have also been found (e.g. Pörtner et al. 2006). The reasoning behind this 'oxygen hypothesis' is that as the size of an organism increases, its surface area:volume ratio reduces. This means that larger animals have more tissue volume requiring oxygen, but relatively less surface area with which to sequester it from the surrounding water. In warmer waters, not only is their less dissolved oxygen, but the oxygen needs of animal tissues is higher. Thus polar gigantism occurs due to cold water temperatures and high levels of dissolved oxygen. However, more recent research involving the self-righting abilities of 12 different-sized species of sea-spider (Woods et al. 2008) did not fully support the oxygen hypothesis, although it did agree that oxygen availability was likely to be one important factor, just not the only one. A possible explanation is that, being an apparently early branch of sea-spider evolution (Arango & Wheeler 2007), Colossendeis species have been adapting to cold, well-oxygenated waters for a longer period that other genera and have oxygen delivery systems which are more finely tuned to such conditions. If this is the case, then climate change is a potentially serious threat to a specialist groups of species functioning with narrow oxygen safety margins i.e. warmer waters leading to higher oxygen demand and lower availability could push Colossendeis beyond these margins more quickly than it can adapt.
So, although it seems that polar gigantism is a result of oxygen availability plus other factors, abyssal gigantism is in some ways more mysterious. Firstly, as noted by Deep Sea News, much work has looked at deep sea dwarfism rather than gigantism because so many taxa show this reduction in size, suggesting that the deep ocean is primarily a small-organism habitat (McClain et al. 2005, Kaariainen & Bett 2010). Thus, the incidence of abyssal gigantism (seen particularly in crustaceans, but also a range of other taxa) contrasts strongly with what appears to be the 'normal' situation in the deep ocean.
Abyssal dwarfism has generally been attributed to low food availability, with most animal communities (away from seeps and vents) relying on the 'marine snow' of detritus sinking from the surface, with occasional larger localised inputs such as dead whales. Thus little food arrives, especially away from productive shallow coastal waters. However, several possible explanations for the rarer gigantism have been proposed e.g.:
- Higher oxygen availability (Chapelle & Peck 2001) as the amount of available oxygen determines the amount of sustainable tissue, with cell size and number both increasing with higher oxygen concentration in Drosophila fruit flies (Frazier et al. 2001) and freshwater amphipods (Peck & Chapelle 2003). In gastropods, a link between larger size and more oxygenated deep-sea sites has been noted (McClain & Rex 2001), but giant isopods Bathynomus sp. are known from low-oxygen regions in the Gulf of Mexico.
- Longer lifespans due to reduced predation (few predators) and slower growth rates in cold water with larger cell size in crustaceans (Timofeev 2001) with a similar process suggested for other taxa (e.g. Van Voorhies 1996).
However, although key effects such as the link between oxygen levels and cell size/number have been described, these are the result of work on unrelated taxa and it remains unclear precisely why Colossendeis sea-spiders (let alone giant isopods) should exhibit gigantism while others do not - and so it is tie for a little (hopefully not too idle) speculation:
- Through development of fat reserves, larger size may allow longer gaps in feeding when food is scarce (although sea-spiders do not appear to have much space for such storage) or larger foraging areas.
- It may be that gigantism is linked to the species' evolutionary past as island biotas also show a mixture of dwarfism and gigantism related to the size of their mainland ancestors (e.g. Lomolino 2005). Could Colossendeis (or Bathynomus) be descendents of larger ancestors from warmer and/or shallower waters and thus display gigantism rather than dwarfism when adapted to polar/abyssal conditions?
- Is their large size actually adaptive or is it simply a random evolutionary trait which happens to serve them as well as dwarfism might?
- With many abyssal species tending towards dwarfism, might it provide a form of niche-separation and thus reduce competition?
- Does large size itself reduce predation?
- Might large size (through the ability to exploit a large food patch or larger food items) reduce the need to move and thus expend energy? Would this be a successful trade-off against the need for more energy/food to maintain a larger body size?
- With the smaller surface area: volume ratio, larger bodies can mean easier temperature regulation, but would this be sufficiently adaptive and if so, why in only a few species?
- With some hydrothermal vent and seep species such as vestimentiferan tubeworms showing great longevity (e.g. Fisher et al. 1997), and gigantism being at least partly associated with slow growth over a long period in a stable, if food-scarce environment, might gigantism be linked to an adaptive function of increased individual longevity in areas away from vents and seeps?
Further reading
For a key to coastal British species: King, P.E. (1986). Sea Spiders. A revised key to the adults of littoral Pycnogonida in the British Isles. Field Studies 6(3): 493-516.
References
Arango, C.P. & Wheeler, W.C. (2007). Phylogeny of the sea spiders (Arthropoda, Pycnogonida) based on direct optimization of six loci and morphology. Cladistics 23: 255–293. Arnaud, F. & Bamber, R.N. (1987). The Biology of Pycnogonida. Advances in Marine Biology 24: 1-96.
Bamber, R.N. & El Nagar, A. (eds.) (2012). Pycnobase: World Pycnogonida Database. [accessed 09/02/2012]
Barnes, R.D. (1980). Invertebrate Zoology (4th ed.). Holt-Saunders, Philadelphia.
Chapelle, G., & Peck L.S. (1999). Polar gigantism dictated by oxygen availability. Nature 399: 114-115.
Fisher, C.R., Urcuyo, I.A., Simpkins, M.A. & Nix, E. (1997). Life in the slow lane: growth and longevity of cold-seep vestimentiferans. Marine Ecology 18(1): 83-94.Frazier, M. R., Woods, H. A. & Harrison, J. F. (2001). Interactive effects of rearing temperature and oxygen on the development of Drosophila melanogaster. Physiological and Biochemical Zoology 74: 641-650.
Kaariainen, J. & Bett, B. (2010). Evidence for benthic body size miniaturization in the deep sea. Journal of the Marine Biological Association of the UK. 86(6): 1339-1345.
Lomolino, M.V. (2005). Body size evolution in insular vertebrates: generality of the island rule. Journal of Biogeography 32(10): 1683-1699.
McClain, C.R & Rex, M.A. (2001). The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression. Marine Biology 139: 681-685.
(2005). Deconstructing bathymetric body size patterns in deep-sea gastropods. Marine Ecology Progress Series 297: 181-187.
Peck, L.S. & Chapelle, G. (2003). Reduced oxygen at high altitude limits maximum size. Proceedings of the Royal Society of London B (Suppl.) 270: S166-167.
Pörtner, H.O., Peck, L.S. & Hirse, T. (2006). Hyperoxia alleviates thermal stress in the Antarctic bivalve, Laternula elliptica: evidence for oxygen limited thermal tolerance. Polar Biology 29: 688-693.
Timofeev, S.F. (2001). Bergmann's Principle and deep-water gigantism in marine crustaceans. Biology Bulletin 28(6): 646-650.
Van Voorhies, W.A. (1996). Bergmann size clines: a simple explanation for their occurrence in ectotherms. Evolution 50: 1259-1264.
Woods, H. A., Moran, A. L., Arango, C. P., Mullen, L. & Shields, C. (2008). Oxygen hypothesis of polargigantism not supported by performance of Antarctic pycnogonids in hypoxia. Proceedings of the Royal Society B 276: 1069-1075.
Wu, N. & Mastro, J. (2004). Under Antarctic Ice. University of California, Berkeley CA.
Monday, 21 November 2011
The eyes have it: Trilobites as models of ecology and evolution
Following my recent scribblings about cave bear dentition, I thought I would make the journey back to looking at extant invertebrates a step at a time. So, staying in the world of palaeonotology, but moving onto invertebrates (slightly more familiar ground), I decided to see if I could derive some more inspiration from my curio shelves. So, given that I've previously written about my Cretaceous water bug, it seemed about time I tackled that most popular of fossil invertebrates, the trilobite. Now, I've only got the one trilobite, but it's quite a good specimen, so here it is in all its glory:
The shape of this, with a bulging and pimply glabella ('forehead') suggests it is in the genus Phacops (possibly P. rana) but not Reedops as this would have a smooth glabella. However, what brings me straight to the suborder Phacopina in the first place is its eyes (see Murray 1985 for a key to trilobite groups).
Trilobite eyes are compound like those of modern invertebrates (well, up to a point) but vary greatly, and this one is known technically as 'schizochroal'. Only found in the Phacopina, and not all of these, eyes of this type have relatively few relatively large lenses as can be seen in the photo. These lenses are well separated and if we took a section through the eye, apart from destroying my trilobite, we would see that each lens had its own cornea (outer layer - which we also have) and was separated from the others by a thick piece of exoskeleton called the sclera with the cornea extending down through this. This is not the case in most trilobites which have 'holochroal' eyes. These have small lenses which are often more numerous and may look more like our familiar 'mosaic' picture of an insect's eye. The lenses all touch each other (i.e. are not separated by sclera) and have a common cornea covering the whole surface of the eye. Lastly, a few trilobites (only the Cambrian Eodiscina) have 'abathochroal' eyes which have few, small lenses which are separated as in schizochroal forms but only have thin sclera and a cornea which stops at the surface of the sclera. Got all that? Well, I've only just worked through the anatony of these eye types and found an excellent summary on S.M. Gon's webpage 'The Trilobite Eye' which I recommend if you would like a expanded and illustrated version of my account here as well as other variant such as stalked eyes and those with inbuilt eyeshades!
Apart from my liking for all things morphological, one important aspect of these eye forms (and those trilobites that were eyeless) is what they can tell us about the life/ecology of trilobites. For example, eye loss is seen in some benthic (bottom-feeding) forms which lived in low-light conditions. So, starting with Phacops, it has fully developed eyes and can be seen as an ancestral form of genera with reduced eye development such as Cryphops which in turn evolved into the eyeless Trimerocephalus. So, we have a genus with well developed eyes which evolved into forms reducing and then losing them - a process that took a long time in human terms but occurred in the, er, blink of an eye, when looking at geological timescales (see Dawkins 1996 for more on the evolution of eyes of various types).
This loss of eyes in a benthic environment is a simple enough concept, but what about the development of schizochroal eyes in the first place? Unlike most (holochroal) trilobite eyes they are highly specialised and have no clear analogue in the modern fauna (Fortey, 2000). Firstly the lenses are crystalline, being made of calcite and are almost spherical, sometimes a little drop-shaped. These lenses have even had photographs taken through them and it is evident that sharp images could be formed and that larger 'pieces' of the trilobite's surroundings would have been visible per lens than for those with holochroal eyes. However, trying to use spherical transparent items such as marbles in a visual system doesn't work well because of 'spherical aberration' - the images become distorted, inverted, fuzzy. However, Phacops solved this problem by making the calcite impure, specifically by replacing some of the calcium atoms in calcite with magnesium and forming an internal 'bowl' in the lens which worked as a corrective structure, separating the eye into two sections of differing refractive index and allowing for the spherical aberration (Clarkson & Levi-Setti, 1975). So, although holochroal eyes would presumably have been good at detecting movement (food, predators?) as is the case in many modern invertebrates, Phacops could see chunks of detail. It is unknown exactly why this type of eye evolved, but it arose, like all other evolved structures, because it improved survival, in this case through a process known as post-displacement paedomorphosis (i.e. the retention of juvenile features - part-developed holochroal eyes are like smaller versions of schizochroal ones).
So, there we have it - Phacops evolved a visual system which has not (yet) been 'repeated', but why did I call trilobites 'models of ecology and evolution' in the title of this article? Well, the evolutionary side is well documented (despite what hordes of frankly bizarre creatonist and Intelligent Design websites might assert to the contrary - however, I won't go there...) both in the scientific literature and in popular-science publishing/broadcasting - despite the hundreds of millions of years that separate trilobites from our modern Earth, they are to some extent familiar. As for the ecology, it allows us to mix some evidence with a dash of speculation. Benthic lifestyles with low light levels led to the loss of eyes and so we can infer something of the 'lifestyles' of genera such as Trimerocephalus from their morphology as well as from the location and material in which they are found. However, in Phacops, we have some evidence of what level of detail they might have been able to see - I say might because their optic nerves are not preserved, thus their 'wiring' remains a mystery as far as I am aware, and by extension so is precisely how they perceived the world.
I'll stop there - I hope you enjoyed that, and please do watch this space for a return to the wonderful world of small beetles soon!
References
Clarkson, E. N. K. & Levi-Setti, R. (1975). Trilobite eyes and the optics of Des Cartes and Huygens. Nature 254: 663-667.
Dawkins, R. (1996). Climbing Mount Improbable. Viking, New York.
Fortey, R. (2000). Trilobite! Eyewitness to Evolution. Flamingo, London.
Gon, S.M. (2007). The Trilobite Eye. http://www.trilobites.info/eyes.htm [accessed 20/11/2011].
Murray, J.W. (ed.) (1985). Atlas of Invertebrate Macrofossils. Longman, London.
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| My trilobite, 5cm long and showing clear segmentation plus its well preserved head on the right. |
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| Phacops compound eye showing clearly separated lenses. This is the right eye looking from above and slightly off to the right. The pimply surface to the left is the fixed 'cheek' area known as the fixigena which appears as a lobe on either side of the glabella. |
Apart from my liking for all things morphological, one important aspect of these eye forms (and those trilobites that were eyeless) is what they can tell us about the life/ecology of trilobites. For example, eye loss is seen in some benthic (bottom-feeding) forms which lived in low-light conditions. So, starting with Phacops, it has fully developed eyes and can be seen as an ancestral form of genera with reduced eye development such as Cryphops which in turn evolved into the eyeless Trimerocephalus. So, we have a genus with well developed eyes which evolved into forms reducing and then losing them - a process that took a long time in human terms but occurred in the, er, blink of an eye, when looking at geological timescales (see Dawkins 1996 for more on the evolution of eyes of various types).
This loss of eyes in a benthic environment is a simple enough concept, but what about the development of schizochroal eyes in the first place? Unlike most (holochroal) trilobite eyes they are highly specialised and have no clear analogue in the modern fauna (Fortey, 2000). Firstly the lenses are crystalline, being made of calcite and are almost spherical, sometimes a little drop-shaped. These lenses have even had photographs taken through them and it is evident that sharp images could be formed and that larger 'pieces' of the trilobite's surroundings would have been visible per lens than for those with holochroal eyes. However, trying to use spherical transparent items such as marbles in a visual system doesn't work well because of 'spherical aberration' - the images become distorted, inverted, fuzzy. However, Phacops solved this problem by making the calcite impure, specifically by replacing some of the calcium atoms in calcite with magnesium and forming an internal 'bowl' in the lens which worked as a corrective structure, separating the eye into two sections of differing refractive index and allowing for the spherical aberration (Clarkson & Levi-Setti, 1975). So, although holochroal eyes would presumably have been good at detecting movement (food, predators?) as is the case in many modern invertebrates, Phacops could see chunks of detail. It is unknown exactly why this type of eye evolved, but it arose, like all other evolved structures, because it improved survival, in this case through a process known as post-displacement paedomorphosis (i.e. the retention of juvenile features - part-developed holochroal eyes are like smaller versions of schizochroal ones).
So, there we have it - Phacops evolved a visual system which has not (yet) been 'repeated', but why did I call trilobites 'models of ecology and evolution' in the title of this article? Well, the evolutionary side is well documented (despite what hordes of frankly bizarre creatonist and Intelligent Design websites might assert to the contrary - however, I won't go there...) both in the scientific literature and in popular-science publishing/broadcasting - despite the hundreds of millions of years that separate trilobites from our modern Earth, they are to some extent familiar. As for the ecology, it allows us to mix some evidence with a dash of speculation. Benthic lifestyles with low light levels led to the loss of eyes and so we can infer something of the 'lifestyles' of genera such as Trimerocephalus from their morphology as well as from the location and material in which they are found. However, in Phacops, we have some evidence of what level of detail they might have been able to see - I say might because their optic nerves are not preserved, thus their 'wiring' remains a mystery as far as I am aware, and by extension so is precisely how they perceived the world.
I'll stop there - I hope you enjoyed that, and please do watch this space for a return to the wonderful world of small beetles soon!
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| As in some modern invertebrates, the rear segments formed a section behind the thorax known as the 'pygidium' AKA 'the end'! |
References
Clarkson, E. N. K. & Levi-Setti, R. (1975). Trilobite eyes and the optics of Des Cartes and Huygens. Nature 254: 663-667.
Dawkins, R. (1996). Climbing Mount Improbable. Viking, New York.
Fortey, R. (2000). Trilobite! Eyewitness to Evolution. Flamingo, London.
Gon, S.M. (2007). The Trilobite Eye. http://www.trilobites.info/eyes.htm [accessed 20/11/2011].
Murray, J.W. (ed.) (1985). Atlas of Invertebrate Macrofossils. Longman, London.
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