Edible Stinkbugs

In recent years, there has been some discussion in certain circles about whether people in western cultures should become more accepting of the practice of entomophagy: that is, eating bugs. For the most part, insects do not play a big part in diets in the English-speaking world except indirectly. In other parts of the world, however, certain insects may be eaten with relish. One such insect is the edible stinkbug Encosternum delegorguei of southern Africa.

Edible stinkbug Encosternum delegorguei, from Dzerefos et al. (2013).

The edible stinkbug is a member of the family Tessaratomidae, one of a number of families in the stinkbug superfamily Pentatomoidea. Tessaratomids are mostly relatively large, flat-bodied stinkbugs, often with shining metallic coloration, found in warmer parts of the world. They are all plant-suckers; one species, the lychee stinkbug Tessaratoma javanica, is a significant pest of lychee crops while the bronze orange bug Musgraveia sulciventris is a pest of citrus trees in Australia. The edible stinkbug feeds on a range of tree species, belonging to a number of different flowering plant families such as Combretaceae, Fabaceae and Ebenaceae. Though widespread in southern Africa, their distribution seems to be patchy; only certain ethnicities have a tradition of stinkbug harvesting (Dzerefos et al. 2013).

Harvester collecting stinkbugs, copyright Cathy Dzerefos.

Edible stinkbugs are collected during winter (the dry season) when they aggregate in large protective clusters (up to football-sized) on particular trees. Like other stinkbugs, Encosternum delegorguei produce a foul-smelling defensive chemical from glands on the thorax. As well as smelling bad, this chemical can stain skin and may cause temporary blindness if it gets into eyes. Dzerefos et al. (2013) note that stinkbug harvesters informed them that exposure to the defensive chemical over several years could cause fingernail loss and wart growth. The chemical needs to be removed from the bugs before they are cooked for consumption because, as one harvester explained, "if you eat the unprepared one it will kill taste for a month".

Clusters of stinkbugs are collected live into bags which are then shaken to encourage the bugs to discharge their chemicals. Further processing could be done by two methods. Perhaps the more common method is to pinch off the head of each bug then squeeze out the contents of the thorax, after which the bugs are cooked immediately. However, the Bolobedu people (who collect stinkbugs more for commercial sale than for their own consumption) place the bugs into a bucket with a perforated base, then pour hot water over them and stir vigorously. The bugs discharge their glands into the water as the heat kills them. They are then rinsed off in cold water, then returned to hot water for about eight minutes, then spread out on bags on the ground to dry. Any bugs that had not fully discharged their glands before dying can be recognised by dark marks on the thorax and are discarded. Though slightly more involved than the waterless method, this process of preparation has the advantage that bugs can be stored for some time rather than having to be cooked immediately. Stinkbugs are usually cooked by braising in a frying pan with salt; they are supposed to have a spicy taste, like chili.

Basket of prepared stinkbugs, from here.

According to Dzerefos et al. (2013), many of the stinkbug harvesters they spoke to reported a decline in populations of the bugs in recent years. Potential reasons for the decline included drought and/or the felling of trees that would otherwise be used by the bugs as roosts. Could edible stinkbugs be more widely used commercially? Perhaps, but it should be noted that while some groups relish the bugs, their neighbours disdain the delicacy. Mind you, Bolobedu people apparently didn't eat the bugs themselves before the 1980s, only taking up harvesting them when co-workers in tea plantations taught them what a resource they had on their hands!

REFERENCE

Dzerefos, C. M., E. T. F. Witkowski & R. Toms. 2013. Comparative ethnoentomology of edible stinkbugs in southern Africa and sustainable management considerations. Journal of Ethnobiology and Ethnomedicine 9: 20.

Publication date of Bulletin de la Société Philomathique

I should say up front, this is going to be a pretty esoteric one. It's just that this is something I spent a fair chunk of a morning trying to work out, and I may as well put what I found up here in case someone else finds it useful.

A few weeks back I found myself, as one does, trying to sort out the exact publication date of early numbers of the Bulletin des Sciences, par la Societé Philomathique de Paris, which has been archived online at the Biodiversity Heritage Library. The Société Philomathique was an association of French scientists and polymaths from a wide range of disciplines founded in 1788. You can find the webpage for the current iteration of the Société here. In 1791, the Societé decided to circulate a bulletin of abstracts of their meetings, including summaries of papers and letters presented there.

The title page of the volume of the Bulletin available at the Biodiversity Heritage Library gives the dates of "Juillet 1791, a Ventôse, An 7", or July 1791 to February–March 1799, which is the dates of the meetings presented therein ("Ventôse, An 7" is a date in the Republican Calendar that was introduced for a period following the establishment of the French Republic in 1792). Citations I could initially find for individual notices in the Bulletin were all attributed to dates of the separate meetings that they were presented at (e.g. something presented at the May 1794 meeting would be cited as "1794"). But it was immediately obvious to me that the notices could not have been published at the times of the original meetings, at least not as they appeared in the volume reproduced, because abstracts from separate meetings would appear on the same page! Hence my search for information on the Bulletin's actual publication date: were notices for individual meetings issued separately at the time, or did they not actually appear in print until the subsequent publication (presumably in 1799 or even later) of the collected volume? I should note that some of the abstracts in the Bulletin included descriptions of new species, so the question of publication date could have further taxonomic implications.

A page from the collated Bulletin, showing how the last entry for the December 1792 meeting is followed immediately by the section for January 1793, without a page-break for originally separate issues to have been collected together.

Eventually, I was able to establish that separate Bulletin issues had indeed been released for each meeting (you can see reproductions of the uncollated originals at Gallica). However, there is a complication. Early issues of the Bulletin were written by hand, and distributed only to the members of the Société (about 18 people at the time). It was not until November 1792 that a printed version of the Bulletin began to be disseminated more widely. Now, the International Code of Zoological Nomenclature requires that any publication for taxonomic purposes produced before 1986 must "have been produced in an edition containing simultaneously obtainable copies by a method that assures...numerous identical and durable copies" (Article 8.1.3). A handwritten manuscript would not meet that requirement, so any zoological name appearing in those early bulletins would not count as published. They would not become established until the subsequent publication of the collated volume, which according to an introduction written by Jonathan Mandelbaum in 1977 for a bound collection of the original Bulletin issues (reproduced at Gallica here) happened in 1802.

Original first page of the Bulletin for January 1793. As well as the separation from the December entries, note that the first entry of the original version has been omitted from the collated version, and that the title's original spelling said 'Philomatique' rather than 'Philomathique'.

As an example of the sort of consequences that might arise from this, consider Odiellus spinosus, a widespread harvestman species found in western Europe. This species was very briefly described, as Phalangium spinosum, by Bosc in 1792 in one of the manuscript issues of the Bulletin de la Societé Philomatique (the February 1792 one, to be exact). This has uniformly been accepted as the publication date, but Bosc's species was not properly published until 1802. This might be a simple question of book-keeping, were it not that, in the meantime, Latreille (1798) had used the name 'Phalangium spinosum' for a quite different harvestman species, and described what is now known as 'Odiellus spinosus' under the name of 'Phalangium histrix'. So strict application of the law of priority means that the species in question should be known as Odiellus histrix.

Fortunately, in this case there may be some loopholes available to us. Latreille's names both have strict priority over Bosc's, but they may each count as nomina oblita ('forgotten names'). This is a provision in the ICZN that a name that has not been used as valid since before 1899 can be set aside in favour of a more widely recognised junior synonym if "the junior synonym or homonym has been used for a particular taxon, as its presumed valid name, in at least 25 works, published by at least 10 authors in the immediately preceding 50 years and encompassing a span of not less than 10 years" (ICZN Art. 23.9.1.2). Latreille's Phalangium spinosum was soon recognised as a synonym of an earlier name, and was last used as valid in 1802. Phalangium histrix (or derived combinations thereof) persisted in the literature for longer, but I haven't come across it being used as a separate species after 1876. The open question is whether Bosc's name has been used often enough to warrant automatic conservation. I suspect it would have (I haven't done a proper tally myself, but a search for 'Odiellus spinosus' on Google Scholar brings up about 130 results) but, if not, then an appeal to the ICZN would be required if we wanted to keep using the current name for the species.

Harden Up, Puffball!

Near my home back in Australia, there's a park where we walk the dog most days. During the summer, when Perth receives little rain, the grass in the park dries off and the ground becomes hard. In some particularly dry spots, ground cover is absent completely (there's a large bare patch that used to house a meat ant colony; the ants died off a few years back but the nest site has never been re-claimed by grass). As autumn approaches, cream-coloured lumps can be seen in these bare patches, pushing their way through cracks in the ground. The lumps eventually crack and split, turning to dust over the course of several weeks. These lumps are Pisolithus puffballs.

Mature Pisolithus 'arhizus' puffballs, copyright Paul Venter.

A long-established system in the classification of basidiomycete fungi (the class of fungi that includes most familiar mushroom-forming species) divided many of the species between two groups, the hymenomycetes and the gasteromycetes. Hymenomycetes (the name means 'membrane fungi') included the classic mushrooms, with spores produced on an exposed membrane on the open fruiting body (often underneath) from which they were expelled when mature. Gasteromycetes ('stomach fungi') were forms such as puffballs in which spore-producing structures were completely enclosed within a sealed fruiting body; these structures would break apart at maturity and only then would the fruiting body open up to release the freed spores. However, while the hymenomycete-gasteromycete division was certainly convenient, it was not entirely watertight. For instance, ink-cap mushrooms were clearly hymenomycetes going by their exposed membranes, but the way their fruiting bodies dissolved to release their spores was more than a little gasteromycete-like. When molecular phylogenetic studies came to be included in the mix, it became clear that the two groups were not phylogenetically distinct. Indeed, the usual poster-children for gasteromycetes, the Lycoperdaceae puffballs, have turned out to be close relatives to the most familiar of all hymenomycetes, the field mushroom Agaricus bisporus. 'Gasteromycetes' have evolved from 'hymenomycete' ancestors on several different occasions; a puffball is basically a mushroom that doesn't open.

When molecular studies came to examine Pisolithus and a number of related 'gasteromycete' taxa, they turned out to be related to the 'hymenomycete' boletes in the order Boletales. Boletes are spongy mushrooms in which the spore-producing section on the underside of the cap is divided into pores rather than gills. Some boletes are highly regarded for their edibility, if you can get to them before other animals and insects that find them equally tasty do (others, however, are toxic, so as always with mushroom-hunting you need to know what you're eating). A new lineage in the Boletales, the Sclerodermatineae, was recognised for Pisolithus and its relatives; this lineage includes some forms that would have been recognised in the past as gasteromycetes and some that would have been called hymenomycetes. As with other members of the Boletales, most if not all members of the Sclerodermatineae are ectomycorrhizal, forming close symbiotic associations with the roots of certain trees. In most cases, these associations are essential to the well-being of both members of the partnership as the two exchange nutrients.

Salmon gum mushroom Phlebopus marginatus, copyright Ian Sutton.

'Hymenomycete' genera of the sclerodermatines include Gyroporus, Boletinellus and Phlebopus. Members of these genera are more or less similar in overall appearance to other boletes, though Boletinellus has thin caps on which the stalk may be displaced to one side rather than central and the pores on the underside are less distinct. Gyroporus boletes may be characterised by features of the stalk, in which the centre has a fluffy section that dissolves over time to leave a hollow core. The fruiting bodies produced by species of Phlebopus can be absolutely massive: weights of up to 30 kg have been recorded for a single mushroom. Boletinellus and Phlebopus (which together form the Boletinellaceae) are remarkable in that their ectomycorrhizae are actually harmful to the trees with which they associate. Hyphae of Boletinellaceae form sheaths or crusts around the roots of trees that are not normally involved in ectomycorrhizal associations (ash in the case of Boletinellus merulioides, various trees such as citrus and coffee in the case of Phlebopus species) that provide a home for aphids or mealybugs. The bugs have a sheltered place to live, and the fungus gains nutrients excreted by the bugs as they feed on the tree roots.

Phylogenetic analyses indicate that the Boletinellaceae are the sister group to other Sclerodermatineae (Wilson et al. 2012) but whether the 'gasteromycete' sclerodermatines are monophyletic to Gyroporus or not is more of an open question. Gasteroid sclerodermatines include the earthballs Scleroderma and the horse dung fungus Pisolithus. Members of these genera have hard, puffball-like fruiting bodies; in the case of Pisolithus, these fruiting bodies are so hard that they may sometimes be seen forcing their way through road asphalt or concrete. Both Scleroderma and Pisolithus have been widely used in inoculating soil for forestry and revegetation, in part because they form ectomycorrhizal associations with a wide variety of tree species. However, more recent studies have suggested that some of this apparent egalitarianism may be due to confusion between cryptic species; individual strains of the two genera may be more host-selective than previously recognised (Watling 2006). Inoculation with the wrong strain might then lead to tree growth not being helped, or even being hindered. Another example of the practical consequences of poor taxonomy!

Barometer earthstars Astraeus hygrometricus, copyright Richard Sullivan.

Similar taxonomic questions surround the barometer earthstars of the genus Astraeus, long recognised as a single cosmopolitan species A. hygrometricus but probably a complex of more localised species. Earthstars have a double-layered covering (peridium) to the fruiting body; the outer layer of the peridium is leathery and splits open when mature into several pointed rays, hence the fungus' vernacular name. A double-layered peridium is also found in the fruiting bodies of another sclerodermatine genus, Calostoma, but in this case the outer layer is gelatinous. The inner layer of the peridium is brightly coloured, and the appearance of the Calostoma fruiting body as the outer layer breaks open has led to the vernacular name of 'prettymouth'.

Mature prettymouth Calostoma cinnabarina, copyright Dan Molter.

Other members of the Sclerodermatineae are less well known. Diplocystis wrightii is a sclerodermatine known from various locations around the Caribbean that produces clusters of small globular fruiting bodies arising from a basal stroma (hyphal mass). As the upper surface of the peridium becomes dry and papery, it splits apart to turn the fruiting body into an open cup. A similar arrangement of clustered, cup-shaped fruiting bodies is known in a fungus species found in Burmese amber, Palaeogaster micromorpha (Poinar et al. 2014), though structural differences argue against a direct relationship between the two. Finally, there are many other unusual 'gasteromycetes' whose affinities remain uncertain; future studies may yet assign further exemplars to the spectrum of sclerodermatine diversity.

Preserved Palaeogaster micromorpha in Burmese amber, from Poinar et al. (2014).

REFERENCES

Poinar, G. O., Jr, D. da Silva Alfredo & I. G. Baseia. 2014. A gasteroid fungus, Palaeogaster micromorpha gen. & sp. nov. (Boletales) in Cretaceous Myanmar amber. Journal of the Botanical Research Institute of Texas 8 (1): 139–143.

Watling, R. 2006. The sclerodermatoid fungi. Mycoscience 47: 18–24.

Wilson, A. W., M. Binder & D. S. Hibbett. 2012. Diversity and evolution of ectomycorrhizal host associations in the Sclerodermatineae (Boletales, Basidiomycota). New Phytologist 194: 1079–1095.

Fusulinoids: Complex Forams of the Late Palaeozoic

Among the most characteristic fossils of the latter part of the Palaeozoic are the group of Foraminifera known as the fusulinoids. These forams, known from around the middle of the Carboniferous to the end of the Permian, can be extremely abundant. Indeed, I get the impression that some fossil deposits are pretty much made of fusulinoids. Fusulinoids did not merely thrive in their environment; they were the environment.

Limestone block dominated by fusulinids, copyright James St John. Field of view is about 3.9 cm across.

Fusulinoids are distinguished from other forams by their test composition, built from minute granules of calcite, and complex internal structure. Externally, fusulinoids (defined here to exclude their forerunners, the endothyroids) were fairly conservative, with a planispiral, usually involute test (that is, each successive whorl covers the last). The last whorl ended on a transverse wall without a defined aperture; instead, the only connection between the interior and exterior of the test was by a series of pores in said wall. Early forms were disc-shaped; later species could be more globular or fusiform. Some of the later fusulinoids also reached gigantic sizes by single-celled organism standards: whereas the earliest fusulinoids were only a fraction of a millimetre across, the late Permian Polydiexodina could be up to six centimetres along their longest axis (Loeblich & Tappan 1964). Internally, fusulinoids had an incredibly complicated and varied structure which I'm not going to go into too much detail about here, primarily because I barely understand a word of it myself. Any description of fusulinoid morphology quickly devolves into madly throwing about terms like chomata, parachomata, spirotheca, tectorium, and the like, and your humble narrator feeling the need to go look at something else.

Cutaway diagram of a fusulinid, showing an example of internal structure, from here.

I have to go into some detail, though, because some features of the fusulinoid wall structure may explain their success. The ancestral state for the fusulinoid test wall involved a thin layer of solid calcite, the tectum. In most species, the inside of the tectum was coated with a thicker, less dense layer. As the test wall becomes more derived, this inner layer becomes more or less translucent, or pierced by tubular alveoli to produce a honeycomb-like appearance. It has been suggested that these modifications may have been adaptations to accomodating symbiotic microalgae, striking a balance between maintaining the protective test and allowing optimal transmission of light. Microalgal associations with fusulinoids may be corroborated by the discovery of minute fossils of probable planktonic relationships such as Ovummuridae preserved within fusulinoid tests (Vachard et al. 2004).

Ecologically, fusulinoids were restricted to off-shore marine habitats, being mostly found preserved in limestones and calcareous shales. They are absent from deposits that would have been formed in brackish water, and while they may be found in sandstones it is debatable whether such occurrences represent life associations or post-mortem transport (Loeblich & Tappan 1964). Fusulinoids would therefore have been ecologically similar to the inhabitants of modern-day photic zone coral reefs, another reflection of their probable co-dependence with photosynthetic microalgae. However, as successful as the advanced fusulinoids were in their time, they did not make it past the massive extinction event at the end of the Permian. This was not the end of giant and complex forams entirely—indeed, some later forms such as the alveolinids would evolve morphologies very similar to those of fusulinoids—but it was the end of these particular giant forams.

REFERENCES

Loeblich, A. R., Jr & H. Tappan. 1964. Treatise on Invertebrate Paleontology pt C. Protista 2. Sarcodina, chiefly "thecamoebians" and Foraminiferida vol. 1. The Geological Society of America and The University of Kansas Press.

Vachard, D., A. Munnecke & T. Servais. 2004. New SEM observations of keriothecal walls: implications for the evolution of Fusulinida. Journal of Foraminiferal Research 34 (3): 232–242.

Hyopsodontids: Little Slinkers of the Palaeogene

The oft-repeated quote about mammalian palaeontology is that it tends to be focused on "the tooth, the whole tooth, and nothing but the tooth". This is primarily the result of pragmatic constraints: because they are much harder than the other bones of the mammalian skeleton, teeth are much more likely to be preserved in the fossil record. There are a great many fossil mammals for which the teeth remain pretty much the only part of the animal known. However, there is no question that this focus tends to limit our understanding of mammalian evolution. On the one hand, the complex morphology of many mammalian teeth means that they provide a wealth of characters for analysis. On the other, the morphology of teeth is heavily influenced by their bearer's diet and lifestyle, meaning that phylogenetically informative features are probably outweighed by the products of ecological convergence.

Reconstruction of Hyopsodus from Savage & Long (1978), via here.

All of which is pretty important background to keep in mind for any discussion of the Hyopsodontidae, a group of small (mostly rat- or weasel-sized) mammals recognised from the Palaeogene, the early part (Palaeocene and Eocene epochs) of the Caenozoic era. Hyopsodontids are generally assigned to the 'Condylarthra', a group of mammals that has long been recognised as one of the classic examples of a 'wastebasket taxon'. Condylarths were originally united as primitive relatives of the ungulates, the hoofed mammals. However, the individual condylarth families themselves have not got much in common otherwise, and (particularly with the current acceptance that 'ungulates' are probably not a monophyletic group) it is hard to come up with a definition for 'condylarths' that amounts to much more than 'medium-sized, unspecialised Palaeogene placentals'.

The hyopsodontids have been recognised as one of the longest-lived groups of 'condylarths', with assigned members extending from close to the start of the Palaeocene right up to near the end of the Eocene. Here again, though, we come up against the question of definition. The majority of taxa that have been aligned with the hyopsodontids are among those known only from teeth. Features of the hyopsodontid dentition include fairly simple incisors and premolars, small canines, and molars that are more or less bunodont (that is, the cusps are rounded or conical and clearly separate from each other rather than being connected by lophs). The problem is that these are all primitive, unspecialised features. Hyopsodontids are therefore defined more by their lack of alternate specialisations than anything positive, making them something of a wastebasket within a wastebasket.

Until recently, the only hyopsodontid known from much in the way of postcranial material was the type genus Hyopsodus, a number of species of which are known from an extended period of the Eocene. Indeed, Hyopsodus was one of the most abundant mammalian genera of its time, accounting for over a quarter of mammalian remains in a number of deposits where it is found (Rose 2006). These remains combine to give a picture of Hyopsodus as a long, low-bodied animal that has been compared in its proportions to a dachshund, a weasel, or a prairie dog. Hyopsodus would have been a ground-hugging slinker of an animal, build for concealment rather than speed. Short claws on the forelegs may be consistent with a certain degree of digging ability, whether in search of buried tubers or to scrape shallow burrows. Overall, Hyopsodus was probably a generalist, able to make a living wherever it may find itself: the real rat of the Eocene.

It was only relatively recently that Penkrot et al. (2008) provided further descriptions of limb-bone material from two other genera associated with the hyopsodontids, Apheliscus and Haplomylus. And despite the dental similarities between these genera and Hyopsodus, their postcranial anatomy indicates a quite different animal. Though small, the apheliscines were relatively long-legged, speedy runners: sprinters rather than slinkers. Penkrot et al. interpreted the apheliscines as relatives of the modern elephant shrews of Africa; whether or not there was a valid phylogenetic connection, the two would have certainly been ecologically similar.

Both Hyopsodus and Apheliscus were included in the broad-scale analysis of early placental phylogeny by Halliday et al. (2017). The results of the analysis corroborate the implications of the postcranial anatomy: despite dental similarities, the 'hyopsodontids' in the broad sense are not a monophyletic group. Over a dozen other genera are known of candidate hyopsodontids, but so long as they are known only from dental characters their true position remains uncertain. Without postcranial data, it seems, we can't handle the tooth.

REFERENCES

Halliday, T. J. D., P. Upchurch & A. Goswami. 2017. Resolving the relationships of Paleocene placental mammals. Biological Reviews 92 (1): 521–550.

Penkrot, T. A., S. P. Zack, K. D. Rose & J. I. Bloch. 2008. Postcranial morphology of Apheliscus and Haplomylus (Condylarthra, Apheliscidae): evidence for a Paleocene Holarctic origin of Macroscelidea. In: Sargis, E. J., & M. Dagosto (eds) Mammalian Evolutionary Morphology: A Tribute to Frederick S. Szalay pp. 73–106. Springer.

Rose, K. D. 2006. The Beginning of the Age of Mammals. JHU Press.