Does A High Population Guard Against Extinction?

Rocky Mountain locusts Melanoplus spretus, from the Minnesota Historical Society.

The Cloud was hailing grasshoppers. The cloud was grasshoppers. Their bodies hid the sun and made darkness. Their thin, large wings gleamed and glittered. The rasping whirring of their wings filled the whole air and they hit the ground and the house with the noise of a hailstorm.

Laura tried to beat them off. Their claws clung to her skin and her dress. They looked at her with bulging eyes, turning their heads this way and that. Mary ran screaming into the house. Grasshoppers covered the ground, there was not one bare bit to step on. Laura had to step on grasshoppers and they smashed squirming and slimy under her feet.

--Laura Ingalls Wilder, On the Banks of Plum Creek

In 1875, the American Midwest experienced the largest single locust swarm ever recorded. It covered an estimated area of 198,000 square miles, considerably larger than the state of California, and the person who estimated its size recorded that it took five days to pass by. The species composing this gigantic swarm was the Rocky Mountain locust Melanoplus spretus, and at the time it was America's scourge. Locust swarms in 1874, following a dry summer, had devastated Midwestern agriculture: crops were destroyed, livestock and people starved to death. After the 1874 swarms, it was estimated that only one family in ten had stored enough food to last the winter. The entire future of the region became uncertain: one homesteader observed that, "Wheat and grasshoppers could not grow on the same land, and the grasshoppers already had the first claim".

But then something extraordinary happened. After 1875, grasshopper numbers began declining. Before thirty years had passed, the Rocky Mountain locust was not merely no longer a significant pest, it had become completely extinct. No individuals of the species have been seen alive since 1902. The reasons for this precipitous decline have been much debated, but a prominent suspect has been the conversion of large areas of prairie into managed farmland.

I was reminded of the locusts by Alex Wild's recent comments on the decline of the monarch butterfly, a species that, while not yet extinct, has had a precipitous decline in recent years in North America. Alex notes that:

I don’t have many photographs of monarchs. A few bland shots of larvae, a handful of adults on flowers. I never felt any urgency. They were as common as dirt. I just sort of assumed monarchs would always be around to photograph later.

Silly me.

The Rocky Mountain locust, of course, is not the only example of a once-abundant species becoming extinct in historic times. The passenger pigeon Ectopistes migratorius and the Carolina parakeet Conuropsis carolinensis are two other well-known examples. September 1st this year will mark the hundredth anniversary of the death of Martha, the last known surviving passenger pigeon, in Cincinnati Zoo.

Population numbers are often used as a heuristic for estimating extinction threat, at least in the popular media, and often influences priorities for conservation efforts. A species with a surviving population of 1000 individuals is considered more endangered than one with 100,000 individuals. But examples such as the Rocky Mountain locust show us that even the most unimaginably abundant of animals may not be immune from sudden population crashes. Conversely, some animals persist despite very low population sizes. The black robin Petroica traversii has survived its population being reduced to only five individuals, including only a single breeding female (granted, its survival has received more than a bit of a helping hand from some very intensive conservation efforts, and is by no means typical).

So my question is this: what is the correlation between population size and extinction risk? How much does a smaller population size increase the risk of extinction, or is it secondary to factors such as habitat disturbance? I'm not implying that I think these questions haven't been asked before (I'm sure that they have), they're just something I've been wondering recently myself.

What is Inula verbascifolia?

By recommendation of the Committee for Spermatophyta (Brummitt 2005), this is. Photograph by L.R.

Inula verbascifolia is a herbaceous, composite-flowered plant from the eastern Mediterranean. It is mostly found in the Balkan region, but it also reaches into south-eastern Italy and Anatolia. It is closely related to another Greek species, I. candida, and the two have been treated as a single species, but they can be distinguished by features of the leaves (Tan et al. 2003).

The reason for my question, though, is that Inula verbascifolia has been the subject of an application to have its name conserved (Tan et al. 2003). The rules for naming organisms are often assumed to be complicated, and to a certain extent they are, but the underlying principles can be summed up into two rules: (1) every species should have one name that is different from all other species, and (2) when two names are in conflict, the older name is the correct one. However, like all rules of life, sometimes the best thing to do is not follow the rules. Maybe using the older name would be too confusing, if the newer name is much the better known. To account for such scenarios, all of the various bodies governing the naming of organisms (there are separate bodies for animals, plants and bacteria) make allowances for researchers on the organisms concerned to apply for the rules to be temporarily set aside in some way.

In the case of Inula verbascifolia, the plant currently known by that name was not the first to be called that. The German botanist Heinrich Haussknecht recognised the Balkan species as Inula verbascifolia in 1895. Prior to that, it gone under the name of Conyza verbascifolia, coined by Carl von Willdenow in 1803. However, in 1813 Jean Poiret of France had used the name I. verbascifolia for a plant growing the gardens of the Jardin des Plantes in Paris that had originally come from the Caucasus. 1813 beats 1895, so under strict application of the rules the name Inula verbascifolia should apply to the Caucasian plant, not the Balkan one. But the Caucasian plant had not been known by this name since 1819, whereas the Balkan plant was well-known by that moniker, so Tan et al. (2003) applied for the Balkan plant to be allowed to keep it.

I should point out that I'm an animal taxonomist by training, so I have only a basic awareness of the rules that apply to naming plants. One thing that interests me in this case is that things would have played out differently had the organisms in question been animals. The Zoological Code differs from the Botanical Code in that it doesn't regard the genus name as an integral part of the species name, so even if a species name is moved between genera, it still takes its priority from when it was first coined. In this case, for the Zoological Code the important date would not be 1895 when Haussknecht transferred verbascifolia to Inula, but 1803 when Willdenow called it verbascifolia in the first place. So under the Zoological Code, Willdenow's verbascifolia would be older than Poiret's verbascifolia, and there would be no need for the former to be specially upheld.

Another difference between the Zoological and Botanical Codes is in the process of deciding on applications. In the Zoological Code, an appointed body of taxonomists (the Commission) directly makes each decision themselves. In the Botanical Code, on the other hand, each application goes to a Committee (there are separate committees for seed plants, algae, fungi, etc.) who then vote on a recommendation whether or not to accept the application. The final decision is not made by the Committee, but is voted on by the attendees of the next International Botanical Congress, a conference that anyone is allowed to attend (if they're willing to pay the attendance fee, of course). In the case of Inula verbascifolia, the Committee on Spermatophyta recommended that the application be accepted (Brummitt 2005), but I don't know if it has been finally voted upon. I also don't know if Congress votes often go against Committee recommendations (I wouldn't expect them to, but passions can run high in the world of taxonomy).

Inula verbascifolia ssp. methanea, photographed by Giorgos Gioutlakis. (Update: Christine K. tells me that this photo has been misidentified. See her comment below.)

Tan et al.'s application had to save more than just the species name. Haussknecht's Inula verbascifolia shows enough variation over its range that it has been divided between five subspecies. The photograph at the top of this post, taken in Italy, shows the type subspecies I. verbascifolia ssp. verbascifolia. The photograph just above shows another subspecies from Greece. But when Tan et al. looked at the original specimens examined by Willdenow, they found that they did not belong to the subspecies that had since come to be known as the type. Therefore, they designated a new type specimen belonging to the recognised type subspecies: otherwise ssp. methanea might have had to be called ssp. verbascifolia, and ssp. verbascifolia would have had to be called something else. It is possible that Willdenow had himself seen a specimen of the type subspecies that has since been lost: according to Tan et al., he gave the distribution of Conyza verbascifolia as Sicily, Greece and Armenia. Tan et al. pointed out that Inula verbascifolia's distribution in Italy is in Gargano, not Sicily, so regarded Willdenow's record as an error. What they had evidently overlooked was that, in 1803, Gargano was still part of the Kingdom of Sicily.

And if you're still around after all of that, then you may find the newest cartoon from xkcd oddly apropos:

REFERENCES

Brummitt, R. K. 2005. Report of the Committee for Spermatophyta: 56. Taxon 54 (2): 527-536.

Tan, K., J. Suda & T. Raus. 2003. (1582) Proposal to conserve the name Inula verbascifolia (Willd.) Hausskn. against I. verbascifolia Poir. (Asteraceae) and with a conserved type. Taxon 52: 358-359.

The Taxonomy of Cow Farts

The organism in the above picture (from Garrity & Holt 2001) may not look particularly remarkable, but this is a very important microbe. This is a thin section of Methanobrevibacter ruminantium, a member of the group of archaebacteria known as the Methanobacteriales (methanogens). Methanobacteriales get their name because they grow by reacting carbon and hydrogen to produce methane. They are found in a variety of habitats, though all are strict anaerobes (they die if exposed directly to oxygen). As suggested by its name, Methanobrevibacter ruminantium was described from the rumen (part of the digestive system) of cattle; it or closely related strains are also known from sheep, and even from the crop of the hoatzin, the South American bird that is the world's closest thing to a flying cow. These are the organisms that make cattle fart.

Climate change is a major issue in modern society, and a lot of questions have been raised about how to mitigate its effects. The most familiar factor in climate change is the burning of fossil fuels, but something else that has been subjected to scrutiny is the role of livestock. Anyone who has spent much time in the company of cattle will tell you that they belch and fart continuously. Methane emissions from livestock may not produce the same volume of greenhouse gases worldwide as fossil-fuel burning, but they still cause concern because methane is a significantly more potent greenhouse gas (litre for litre) than carbon dioxide. Methane production can also siphon off 10% or more of the energy contained in the livestock's feed, energy that might otherwise go towards putting on weight, making it a concern for the farmer as well as for the environment. As a result, the question has been raised of whether it would somehow be possible to get the world's cattle to effectively put a cork in it.

Unfortunately, it is not as simple as wiping the methanogens from the cattle's system, because they do have a very important role to play. The digestive system of cattle and other ruminants contains a whole ecosystem of micro-organisms that serve to break down the cellulose and other parts of the cattle's food that it can't digest alone. Ciliates in the rumen that break down cellulose excrete hydrogen gas, in the way that we breathe out carbon dioxide as a result of our own respiratory processes. But just as we would not be able to keep functioning if the concentration of carbon dioxide in a room got too high, these cellulose-digesting microbes become sluggish as the concentration of hydrogen in the gut increases. By converting the hydrogen to methane, the methanogens keep the rumen sweet-smelling and fresh (at least by ciliate standards). Without this process of hydrogen removal, the cattle themselves would not survive long.

Comparison of methanogen populations in low-methane (left) and high-methane (right) cattle, from Zhou et al. (2009).

And this is where taxonomy becomes important. I've been talking as if there is only a single methanogen species in cattle. This is not the case. Methanobrevibacter ruminantium is one of at least five Methanobrevibacter species known from cattle rumens, together with a number of methanogen species belonging to other genera (Zhou et al. 2009). And not all these methanogens are equal in the amount of methane they produce. Zhou et al. (2009) compared the methanogen flora in cattle that absorbed a high ratio of nutrients from their food, and produced relatively little methane, with that in cattle that were less efficient digesters and that produced more methane. They found that while members of both groups contained similar total numbers of methanogens, they differed in taxonomic composition. In the high-efficiency cattle, M. ruminantium made up a higher proportion of the gut flora, while other methanogens such as Methanobrevibacter sp. 'AbM4' increased in abundance in low-efficiency cattle.

Now obviously, there's a lot this doesn't tell us. We don't know whether the high-efficiency cattle produce less methane because of the differences in their methanogen flora, or whether the methanogen flora is different because the cattle are more efficient digesters. If the former, then maybe cattle could be inoculated against undesirable methanogens and the less injurious methanogens encouraged. If the latter, then maybe breeding would have to come into it. Or the methanogen flora could differ due to differences in the cellulose-digesting flora, in which case control measures would have to act at that level. Whatever the reasons, the simple fact that there are different species involved is yet another reminder: even if we're talking about climate, taxonomy matters.

REFERENCES

Garrity, G. M., & J. G. Holt. 2001. Phylum AII. Euryarchaeota phy. nov. In: Boone, D. R., R. W. Castenholz & G. M. Garrity (eds) Bergey’s Manual of Systematic Bacteriology, 2nd ed., vol. 1. The Archaea and the Deeply Branching and Phototrophic Bacteria, pp. 211-355. Springer.

Zhou, M., E. Hernandez-Sanabria & L. L. Guan. 2009. Assessment of the microbial ecology of ruminal methanogens in cattle with different feed efficiencies. Applied and Environmental Microbiology 75 (20): 6524-6533.

The Litopterns: Macrauchenia and More

Much has been made of the "splendid isolation" of South America for a large part of the Cenozoic. Finding itself girt by sea, South America became home to a number of endemic groups of animals: the 'terror-birds' of the Phorusrhacidae, notoungulates that were something like a rhino and something like a rabbit, and giant armadillos and anteaters. Among these uniquely South American animals were the subjects of today's post, the litopterns.

Digital reconstruction of Macrauchenia by Deskridge.

Litopterns are one of those groups of animals that tend to be represented in recent popular media by a single example, which many of you may recognise in the picture above. This was Macrauchenia patachonica, one of the latest surviving litopterns (like many other South American taxa, litopterns did not fare well during the so-called Great Faunal Interchange when South and North America became connected). But as with so many other under-represented groups, the popular exemplar is not necessarily a prime example. Macrauchenia was not only one of the last litopterns, it was also one of the largest, and the litopterns came in a whole range of appearances.

The earliest litopterns are known from the late Palaeocene. The basalmost members of the group are classified as the Protolipternidae, but the members of this family are united by primitive characters only. It is generally accepted that litopterns were closely related to two Palaeocene families of South American 'condylarths', the Didolodontidae and Sparnotheriodontidae, and there is a certain degree of arbitrariness about whether or not these families should also be treated as litopterns. Those who would exclude the didolodontoids from the litopterns do so on the basis of the latter's tarsal morphology, which has become adapted for a more cursorial lifestyle. The protolipternids bridge the gap between didolodontoids and other litopterns in that they possessed a litoptern-like tarsus, but retained teeth more like the didolodontoids. Protolipterna also retained five toes on the feet, while this number was reduced in later litopterns (Bastos & Bergqvist 2007). The other noteworthy feature of protolipternids was that they were not very big. Rose (2009) includes an illustration of partial upper and lower jaws of the protolipternid Asmithwoodwardia whose scale bar indicates that the complete skull must have been less than five centimetres in length, or about the size of a brown rat. Cifelli (1983) suggested on the basis of their small size that these animals may have been more leapers than runners, a suggestion not directly supported but not entirely ruled out by Bastos & Bergqvist (2003).

Reconstruction of Thoatherium minusculum by Charles R. Knight.

The remaining litopterns mostly belong to the families Proterotheriidae, Adianthidae and Macraucheniidae, united by specialisations of the dentition and reduction of the number of toes to three (a fifth family, the late Palaeocene Notonychopidae, are represented by dental remains only). The Palaeocene to Pleistocene Proterotheriidae have attracted a reasonable amount of interest in the past because of their convergences with the horses in the Northern Hemisphere. Like horses, proterotheriids centred locomotion on the middle toe only, with the toes on either side being reduced. In the Miocene proterotheriid Thoatherium, the side toes were almost completely lost, reduced to splints even smaller than those of the modern horse (being by this measure more horse-like than an actual horse, Thoatherium has also been a popular subject for books on evolution). In other respects, however, proterotheriids were not so horse-like. With relatively low-crowned teeth, proterotheriids and other litopterns were browsers rather than grazers, and they may have preferred more wooded terrain rather than grasslands. Ecologically, proterotheriids were probably more like deer or small antelopes than horses, and they resembled small antelopes in size. Only one proterotheriid survived into the Pleistocene, Neolicaphrium recens, and only in Uruguay and northern Argentina (Ubilla et al. 2011).

The Adianthidae were small litopterns (though not as small as the protolipternids) known from the Eocene to the Miocene. Most adianthids are known only from dental remains and/or jaw fragments, though some limb bones are known from the Miocene Adianthus godoyi (Cifelli 1991). These indicate a gracile form, probably more similar to proterotheriids than to macraucheniids, though Cifelli noted the similarities to the former were likely related to size rather than indicative of any deeper affinity.

Reconstruction of the cramaucheniine macraucheniid Theosodon garretorum, with the carnivorous metatherian Borhyaena tuberata, by Charles R. Knight.

The Macraucheniidae retained three functional toes, with the middle toe not substantially larger than the two side ones. They also differed from the proterotheriids in the development of a longer neck, and have usually been compared to camels in appearance (the name 'Macrauchenia' was originally coined to effectively mean 'big llama', in the mistaken belief that it represented an ancestor of that animal). They have been divided between to subfamilies, the Oligocene to Miocene Cramaucheniinae and the late Miocene to Pleistocene Macraucheniinae, though the latter are undoubtedly descended from the former. The cramaucheniines retain a plesiomorphic anterior nasal opening, but in the Macraucheniinae the nasal bones are reduced and the nasal opening has moved posteriad on the skull (Dozo & Vera 2010). It is this dorsal position of the nasal opening that has lead to the interpretation of Macrauchenia as having some form of proboscis, like that of a tapir. The combination of a long neck and a proboscis is, however, an unusual one, and I've wondered if it may have been more of a prehensile upper lip. The macraucheniids did better in the Pleistocene than the proterotheriids, with three species described from a large chunk of the continent, but eventually they two went the way of the toxodont.

REFERENCES

Bastos, A. C. F., & L. P. Bergqvist. 2007. A postura locomotora de Protolipterna ellipsodontoides Cifelli, 1983 (Mammalia: Litopterna: Protolipternidae) da Bacia de São José de Itaboraí, Rio de Janeiro (Paleoceno superior). Anuário do Instituto de Geociências 30 (1): 58-66.

Cifelli, R. L. 1983. Eutherian tarsals from the Late Paleocene of Brazil. American Museum Novitates 2761: 1-31.

Cifelli, R. L. 1991. A new adianthid litoptern (Mammalia) from the Miocene of Chile. Revista Chilena de Historia Natural 64: 119-125.

Dozo, M. T., & B. Vera. 2010. First skull and associated postcranial bones of Macraucheniidae (Mammalia, Litopterna) from the Deseadan Salma (late Oligocene) of Cabeza Blanca (Chubut, Argentina). Journal of Vertebrate Paleontology 30 (6): 1818-1826.

Rose, K. D. 2009. The Beginning of the Age of Mammals. JHU Press.

Ubilla, M., D. Perea, M. Bond & A. Rinderknecht. 2011. The first cranial remains of the Pleistocene proterotheriid Neolicaphrium Frenguelli, 1921 (Mammalia, Litopterna): a comparative approach. Journal of Vertebrate Paleontology 31 (1): 193-201.

Paracomatula: Feather Star, or Feather Star Wannabe?

Fossilised accumulation of Paracomatula helvetica, from here.

Earlier posts on this site have discussed examples of the feather stars, the most successful representatives in the modern environment of the crinoids. Originally a group whose members lived permanently attached to the substrate by a stalk, at some point crinoids diversified to a more mobile (or least shiftable) lifestyle, discovering the joys of travel. This was not, it should be noted, an entirely direct process. Many stalked crinoids are also mobile, able to detach themselves from their substrate and crawl to a new position. Other crinoids than the feather stars lost their stalks. And at least one group within the feather stars, the Mesozoic Thiolliericrinidae, reverted back to retaining as adults the larval stalk that most feather stars lose in the course of development.

Nevertheless, the feather stars had definitely made their appearance by the early Jurassic. One of the earliest taxa that has been assigned to the feather stars is Paracomatula, which is known from the very late Triassic to the middle Jurassic (Hess 2013). Paracomatula would have largely resembled a modern feather star in appearance, but had one significant difference. In modern feather stars, the base of the central cup is formed by a large conical plate known as the centrodorsal. In Paracomatula, however, the centrodorsal is replaced by a stack of five narrow plates. These correspond to much-shortened versions of the columnals that make up the stalked in other crinoids, and Rasmussen (1978) and other authors suggested that Paracomatula's separate columnals became fused to form the centrodorsal of the feather stars proper.

However, not all authors have accepted this interpretation. Hess (2013) has argued that details of the development of modern feather stars from a stalked juvenile to a free-living adult indicate that the centrodorsal is derived from the enlargement of a single columnal rather than the fusion of a series. In the earliest definitive feather star, the Jurassic Palaeocomaster, the cirri (tentacle-like appendages) on the centrodorsal are arranged in a haphazard fashion consistent with their development on a single expanding plate, while Paracomatula has a more orderly array of one ring of cirri per columnal without the development of supernumerary cirri. Hess therefore argues that Paracomatula species were not the forebears of feather stars, but their rivals: a closely related group that was independently experimenting with a stalk-free way of life.

REFERENCES

Hess, H. (in press, 2013) Origin and radiation of the comatulids (Crinoidea) in the Jurassic. Swiss Journal of Palaeontology.

Rasmussen, H. W. 1978. Articulata. In: Moore, R. C., & C. Teichert (eds) Treatise on Invertebrate Paleontology pt T. Echinodermata 2: Crinoidea, vo. 3, pp. T813-T927. The Geological Society of America, Inc., and The University of Kansas Press.

The Hydrobiinae: North Atlantic Mud-snails

The fine-looking animal above (photographed by Roy Anderson) is Hydrobia acuta neglecta, a member of the subfamily Hydrobiinae of the family Hydrobiidae. Most members of the Hydrobiidae are freshwater snails (another hydrobiid has been covered on this site here), but Hydrobia and genera closely related to it are found in brackish or marine environments. They are grazers on algae and detritus, and can be very abundant. The group is found in coastal, muddy regions on either side of the North Atlantic, extending on the European side through the Mediterranean and into the Black Sea. Hydrobiids as a whole are not well-studied animals, mostly for one ultimate reason: they're really tiny. Most hydrobiids are only a few millimetres in length. And coupled with that small size is a strong conservatism in external appearance. Compare Hydrobia acuta neglecta above with another hydrobiine, Ecrobia ventrosa, also photographed by Roy Anderson:

The external shell of a hydrobiid supplies few details to distinguish and classify taxa, and dissecting out a snail that small to examine its soft parts is no cake-walk.

Monophyly of the saltwater hydrobiids is supported by molecular data (Wilke et al. 2013), and they form the core of the Hydrobiinae. Bouchet et al. (2005) also listed the family-group taxa 'Pyrgorientaliinae' and 'Pseudocaspiidae' as synonyms of Hydrobiinae. These were both established for freshwater species: the Pyrgorientaliinae for two genera from Turkey, and Pseudocaspiidae for two genera from central Asia (Kabat & Hershler 1993). Whether these taxa are truly associated with the hydrobiines, I suspect, requires further investigation (it should also be noted that many other authors have used 'Hydrobiinae' to refer to more extensive groupings included taxa listed by Bouchet et al. as separate subfamilies).

REFERENCES

Bouchet, P., J.-P. Rocroi, J. Frýda, B. Hausdorf, W. Ponder, Á. Valdés & A. Warén. 2005. Classification and nomenclator of gastropod families. Malacologia 47 (1-2): 1-397.

Kabat, A. R., & R. Hershler. 1993. The prosobranch snail family Hydrobiidae (Gastropoda: Rissooidea): review of classification and supraspecific taxa. Smithsonian Contributions to Zoology 547: 1-94.

Wilke, T., M. Haase, R. Hershler, H.-P. Liu, B. Misof & W. Ponder. 2013. Pushing short DNA fragments to the limit: phylogenetic relationships of ‘hydrobioid’ gastropods (Caenogastropoda: Rissooidea). Molecular Phylogenetics and Evolution 66 (3): 715-736.