Field of Science

Boreonectes: Diversity Hidden Underwater

The beetle in the photo below (copyright Joakim Pansar) may or may not be Boreonectes griseostriatus. This small diving beetle, a few millimetres in length, has been regarded in the past as widespread with a distribution spanning the Holarctic region. However, in recent years it has become apparent that this single widespread species may actually be a number of more localised species in a skin.

This possibility had been considered for a while. In 1890, a Norwegian entomologist recognised distinct montane and coastal species, noting a tendency for the former to the neatly striped whereas the latter was more blotchy. Later authors, however, rejected this distinction. In 1953, a Russian author expressed the view that B. griseostriatus "varies markedly in many characters; all attempts to establish subspecies and varieties are unjustified, because almost all varieties are connected by transitions" (Angus et al. 2015). In its overall appearance, B. griseostriatus is a a fairly undistinguished small diving beetle. Most of the body surface is densely and finely punctate both dorsally and ventrally, and it lacks some of the modifications found in other diving beetles such as lateral grooves on the pronotum or sucker-hairs on the male tarsi (Angus 2010). This latter feature, offhand, is an adaptation that assists males who have it in clinging to the backs of females during mating. Their functionality would be much reduced in punctate species such as B. griseostriatus because the the uneven surface of the female would prevent the suckers from getting a grip, and phylogenetic studies suggest that their absence in Boreonectes may represent a secondary loss. I don't know if the Boreonectes males do anything to make up for their absence; maybe they just have to grip tighter.

Variation in parameres from male genitalia of the Boreonectes griseostriatus group, from Dutton & Angas (2007).

The complicated nature of B. griseostriatus' identity became really apparent in the 2000s when karyotypic studies on European specimens identified several different chromosomal races, distinct not only in chromosome topography but also in number, that may represent distinct species. The original B. griseostriatus of lowland Sweden possesses a karyotype of thirty pairs of autosomal chromosomes plus the X sex chromosome (sex is determined in this genus by an X0/XX system where males have one copy of the X chromosome and females have two, with no Y chromosome). Boreonectes multilineatus, the Scandinavian montane species, has 28 autosomal pairs. Other species have fewer. It appears likely that a similar thing is happening in Boreonectes to the situation I described in an earlier post for the bat genus Rhogeessa where mutations lead to chromosomes becoming fused or split. It is notable in this regard that Angus (2010) found several specimens of B. ibericus from Morocco that were heterozygous for a chromosomal fusion, so that a single fused chromosome was paired meiotically with distinct chromosomes 1 and 24.

Externally, however, these genetically distinct species remain all but indistinguishable. There may be a tendency for one species to be larger than another, or towards slightly different genital morphologies, but these differences are not distinct enough or consistent enough to provide a reliable guide to identification. Which, if you don't have access to fresh specimens allowing a karyotype spread, is a problem.


Angus, R. B. 2010. Boreonectes gen. n., a new genus for the Stictotarsus griseostriatus (De Geer) group of sibling species (Coleoptera: Dytiscidae), with additional karyosystematic data on the group. Comparative Cytogenetics 4 (2): 123–131.

Angus, R. B., E. M. Angus, F. Jia, Z.-N. Chen & Y. Zhang. 2015. Further karyosystematic studies of the Boreonectes griseostriatus (De Geer) group of sibling species (Coleoptera, Dytiscidae)—characterisation of B. emmerichi (Falkenström, 1936) and additional European data. Comparative Cytogenetics 9 (1): 133–144.

Rhampsinitus Re-Redux

I've featured the African harvestman genus Rhampsinitus on this site twice before, but I'm going to have another dive into it today. There's still more I can say about this remarkable genus.

Male Rhampsinitus, possibly R. leighi, copyright Peter Vos. The individual ahead of the male is another Rhampsinitus, probably a female; there's also a short-legged harvestmen beneath the male.

There's more I could say about African phalangiids in general, in fact. There's never been a proper phylogenetic study of the long-legged harvestman family Phalangiidae, so we can't speak with confidence about the relationships between the African members of this group and their relatives elsewhere, but it would not be unexpected if the sub-Saharan phalangiids form an evolutionarily coherent group. Many of the family's most striking exemplars are to be found on the African continent: Cristina with their thick, spiky front legs; sleek, flattened Odontobunus, Guruia with their chelicerae like a pair of jar tongs held in a boxing glove. Rhampsinitus' current position as the best-known African harvestman genus is probably due not only to its diversity but also to its more temperate centre of distribution placing it closer to researchers than these other more equatorial genera.

As mentioned in my first post on the genus, there are currently over forty recognised species of Rhampsinitus. As alluded to in my second post, that number might be expected to change in the future. No reliable identification key is currently available for Rhampsinitus, nor is the information available for many species that would allow such a key to be written. A key to the southern African species was provided by Kauri (1961) but, while I did find this key invaluable when I conducted my own tentative foray into rhampsinitology, I couldn't recommend it to a novice. Kauri was simply unaware of the extreme variation that can be found among male Rhampsinitus belonging to a single species. There are only a handful of species for which both major and minor males have been described and, as I explained previously, minor males may not be identifiable to species without examining genitalia.

Probably a male Rhampsinitus vittatus, copyright Nanna.

This, obviously, is a problem for the handful of species that have been described from what appear to be minor males. Some of these, such as Rhampsinitus fissidens and R. hewittius, are probably doomed to remain mysteries at least until someone redescribes their types. Others may be more recognisable. Rhampsinitus qachasneki is an unusually spiny species described from the mountains of Lesotho, with some of the denticles along the front edge of the body multi-pointed. These distinctive denticles, like repurposed muntjak antlers, might reasonably be expected to be present in any major males of this species, if they exist. The challenge may be even greater for the handle of species that have been described from females. Nevertheless, the known female of R. maculatus, another Lesotho mountain species, has a distinctive spotted colour pattern and thick, remarkably hairy pedipalps that might be expected to show their analogues in the unknown males (again, if they exist: we're kind of glossing over the point that some harvestmen species are known to be parthenogenetic, because harvestmen systematics is so heavily predicated on male genital morphology that the idea of an all-female harvestman species is a trifle intimidating*).

*I assume that this is precisely what Zappa had in mind when he got to the end of Thing-Fish.

Then, of course, there's the persistent question of Rhampsinitus lalandei. This was the first species included in Rhampsinitus in 1879 and as such represents the type or sine qua non of the genus. As was not unusual for the time, its author Eugene Simon was a bit vague about where his original specimen(s) had come from, giving the locality as simply 'Cafrerie'. Cafrerie, rendered in English as Kaffraria or Kaffirland, is a geographical designation that has fallen out of favour these days for reasons I would hope to be obvious, but was commonly used during the 1800s to refer to the area around the eastern coast of modern South Africa, particularly around Port Elizabeth. Unfortunately, Simon's description of R. lalandei is not definitive by modern standards—most of the features described could apply to any number of Rhampsinitus species—and Simon's original specimen appears to have been lost. This presents a problem for any who would suggest that this large genus should be divided up as it might become uncertain which division represents the true Rhampsinitus. Starega (2009) suggested that R. lalandei might be the same as R. crassus, a species definitely found in the Port Elizabeth region. However, it should be noted that Simon described R. lalandei as being irregularly armed with denticles dorsally. In the majority of Rhampsinitus species, the denticles on the opisthosoma form very neat transverse rows, but in others they are a bit more messily placed. Rhampsinitus crassus is one of the former species but the description of R. lalandei suggests it may have been one of the latter. So if anyone's looking at harvestmen from around that area, keep your eyes open.


Kauri, H. 1961. Opiliones. In: Hanström, B., P. Brinck & G. Rudebeck (eds) South African Animal Life: Results of the Lund University Expedition in 1950–1951 vol. 8 pp. 9–197. Almqvist & Wiksells Boktryckeri Ab: Uppsala.

Staręga, W. 2009. Some southern African species of the genus Rhampsinitus Simon (Opiliones: Phalangiidae). Zootaxa 1981: 43-56.


Apart from the mostly terrestrial radiation of the tetrapods, the vast majority of today's bony-skeletoned fishes belong to the clade of the teleosts. Way back in the Triassic, the ancestors of this clade went through a process of modification of the jaw skeleton to make it more mobile and adroit in catching small prey, and this together with a tendency towards the lightening of the skeleton and the body's covering of bony scales marked the beginnings of what is now well over 25,000 species. But while they may pale in comparison to this phylogenetic behemoth, there are still non-teleost (and non-tetrapod) bony fishes out there if you look in the right places.

Alligator gar Atractosteus spatula, copyright Stan Shebs.

Most studies on fish phylogeny in the last decade or so have agreed that the living sister group of the teleosts is the Holostei, a clade including only eight living species. One of these is the bowfin Amia calva, an elongate, cylindrical-bodied fish with a long dorsal fin running most of the length of its back. The other seven sepecies belong to the gar genera Lepisosteus and Atractosteus, forming the family Lepisosteidae*. Gars are also elongate like the bowfin, albeit without the long dorsal fin, and have elongate, flattened jaws (tending to be narrower in Lepisosteus than Atractosteus). The tail fin in both bowfins and gars is rounded, not forked. Living holosteans are restricted to North America (including Central America and the Caribbean)** but fossils show them to have been more widespread in the past. They are mostly found in fresh water; some species may tolerate brackish or even salt water but they do not stay there permanently. Bowfins and gars are able to breathe air directly as well as through their gills (indeed, gars are reported to drown if prevented from coming to the surface for several hours) and can therefore survive in more stagnant waters than many other fish. The bowfin averages about half a metre in length; the smaller gar species are also in this range. The largest species, the alligator gar Atractosteus spatula, reaches at least close to three metres. Larger sizes (up to six metres or more!) have been reported for this species but appear likely to be errors or exaggerations; as noted by one authority, "All fishes shrink under the tape measure" (Grande 2010).

*The incorrect alternative spellings Lepidosteus and Lepidosteidae (as well as Lepidosteiformes) have often appeared in the past.

**References to a supposed Chinese gar have long persisted in the literature, based on a description of a "Lepidosteus sinensis" from 1873. This description was based on a drawing rather than an actual specimen, and it is now thought that the fish depicted was probably a belonid (an unrelated long-jawed teleost) rather than a gar.

Bowfin Amia calva sharing a tank with largemouth basses, copyright Bemep.

Modern holosteans are ambush predators, feeding on other fish or aquatic invertebrates. In general, larger species tend to prefer a diet of fish whereas smaller species focus on invertebrates, but all appear to be happy to take whatever they may, whether alive or dead. The alligator gar has been claimed to attack humans but no such attacks seem to have been authenticated; Grande (2010) stated that "swimmers probably have very little to fear from them". As well as their sheer size, this accusation may have been fueled by the alligator gar's apparent tendency in some areas to hang around wharves scavenging garbage. Neither bowfins nor gars are of high importance as food fish for humans though their size and strength gain them some attraction as sport fish*. An industry for the production and marketing of bowfin roe has arisen in recent years following the decline in availability of caviar from Russian sturgeon species; no such market exists for gar eggs, which are toxic to humans. Historically, the thick armour of scales covering the skin of gars was used by Caribbean Indians for making breastplates while individual scales could be used for arrowheads.

*Grande (2010) quotes Eberle (1990) to the effect that gars have "a poor reputation among anglers, who believe [they] would have been better suited as land dwellers had they been able to stand their own reflections in the water".

Shortnose gar Lepisosteus platostomus, copyright Rufus46.

Reproductive habits are best known in the bowfin and the longnose gar Lepisosteus osseus. Male bowfins construct a nest in mats of fibrous vegetation, into which they attempt to induce passing females to spawn. Guarding of the eggs after spawning is the duty of the male alone; the female moves on, perhaps to spawn in another male's nest (the male himself may also court more females). The eggs are adhesive and take about a week and a half to hatch. Following hatching, the fry attach themselves to nearby vegetation by an adhesive organ at the end of their snout and spend some time being nourished by the remains of their yolk sac beofre beginning to forage. The male will continue to guard his fry until they reach about a month of age. Reproduction in longnose gars is similar in the production of adhesive eggs and the early sessile, snout-attached period of the life cycle, but differs in that there is no nest construction or parental care. There is a record of gar eggs being deposited in the nest of a smallmouth bass and the fry being subsequently raised cuckoo-wise by the nest's owner, but it is unclear whether this reflects any deliberate action by the parental gars or simply a fortuitous accident. Gars take up to six years to reach maturity, with males maturing a couple of years earlier than females.

Semionotus bergeri, copyright Ghedoghedo.

The fossil record of holosteans extends back to their divergence from the teleosts in the early to mid-Triassic, with the bowfin and gar lineages apparently diverging from each other not long afterwards. As noted above, both lineages include a diversity of extinct members that somewhat belies their current paucity, such as Macrosemiidae and Semionotidae in the gar lineage, and Ophiopsidae, Ionoscopidae, Caturidae and Sinamiidae in the bowfin lineage. The greatest diversity in both lineages was during the Jurassic and Cretaceous (Brito & Alvarado-Ortega 2013; Cavin 2010) and the two modern gar genera appear to have been separate lineages at least since the late Cretaceous (Grande 2010). Holosteans were also more ecologically diverse in the past. Masillosteus, a gar genus from the Eocene of Europe and North America, had a shorter jaw and flatter teeth than modern jaws, and probably fed on harder-shelled animals such as molluscs and/or crustaceans. The Mesozoic 'Semionotidae', suggested by Cavin (2010) to be paraphyletic to the gars, were even more diverse, including marine as well as freshwater forms, and forms that may have plant feeders or detritivores. In the early Jurassic of eastern North America, one group of semionotids underwent a lake-based radiation that has been compared to the modern cichlids of African rift lakes. Adequately covering the diversity of fossil holosteans would make this post considerably longer than it already is; perhaps one day, I'll get to it.


Brito, P. M. & J. Alvarado-Ortega. 2013. Cipatlichthys scutatus, gen. nov., sp. nov. a new halecomorph (Neopterygii, Holostei) from the Lower Cretaceous Tlayua Formation of Mexico. PLoS One 8 (9): e73551.

Cavin, L. 2010. Diversity of Mesozoic semionotiform fishes and the origin of gars (Lepisosteidae). Naturwissenschaften 97: 1035–1040.

Grande, L. 2010. An empirical synthetic pattern study of gars (Lepisosteiformes) and closely related species, based mostly on skeletal anatomy. The resurrection of Holostei. Copeia 2010 (2A): iii–x, 1–871.

Canterbury Bells

Bellflowers or harebells are one of the classic plants associated with the English country garden. For today's post, I'll be covering the family of plants that bellflowers belong to.

Fairy's thimble Campanula cochleariifolia, copyright Jerzy Opioła.

The Campanulaceae are a family of over 2300 plant species found almost worldwide (Crowl et al. 2016). The family is, however, divided between five subfamilies that some authors would treat as separate families, in which case 'Campanulaceae' would be restricted to the 600 or so species of the subfamily Campanuloideae. It is this subfamily that includes the bellflowers. The vernacular name, of course, refers to the shape of the flowers produced by these plants, as indeed does the botanical name: Campanula translates as 'little bell'. These flowers are radiately symmetrical with all petals more or less the same size and shape and evenly arranged in a circle. Other subfamilies of the Campanulaceae in the broad sense, the largest of which is the lobelias of the Lobelioideae, produce more bilaterally symmetrical flowers with petals differing in size and/or with some petals closer together than others. Fruits are most commonly a capsule, with the seeds dispersed by wind, but some lobelioids produce fleshy fruits that attract birds. The lobelioids are most diverse in the southern continents, and it is thought that this may have been the original home of the family as a whole when it arose sometime close to the end of the Cretaceous, possibly in Africa. At some time in the early Cenozoic, however, the campanuloids arrived in and underwent a significant radiation in the Palaearctic. This dispersal may be related to the different flower morphology of the campanuloids, as they adapted from the bird, bat and butterfly pollinators of the tropics to the bee and fly pollinators of more temperate habitats.

Glandular threadplant Nemacladus glanduliferus var. orientalis, copyright Stan Shebs.

The genetics of Campanulaceae, specifically of their chloroplasts, should also not go unnoticed. The structure of the chloroplast genome in plants is usually very stable, with few changes in gene arrangement and order. However, at various points in the history of Campunulaceae, large chunks of foreign DNA have been inserted in the original plastid chromosome, with a number of these insertions also associated with inversions in the direction of adjoining sections of the original genes (Knox 2014). This kind of insertion is unique among flowering plants: changes in the gene content of plastids more usually involve genes being transferred out of the plastid. The source of this extra DNA is uncertain: it may have come from the plant's own nucleus, or it may have come from an as-yet-unknown endosymbiont. Also unknown is the functional significance of these rearrangements, if any. Some insertions have clearly resulted in pseudogenes, with their sequences rapidly breaking down through subsequent genetic drift. But others have preserved the structure of functional genes, suggesting continued selection for their retention.

Cyanea duvalliorum, an arborescent Hawaiian lobeliad, copyright Forest & Kim Starr.

The majority of Campanulaceae are small perennial herbs. Two genera of distinctive enough to be assigned to their own subfamilies include annual herbs: the threadplants Nemacladus of southwestern North America, and the little-known Chilean Atacama desert endemic Cyphocarpus. Some members of the Lobelioideae are woody subshrubs, and at some point one of these woody lobelioids managed to make its way to the Hawaiian archipelago where it gave rise to one of the world's most remarkable insular radiations, and the single largest such radiation in plants. Over 120 species of lobeliads are known from the Hawaiian islands, varying from single-stemmed succulents to straggling vines to trees over 18 metres in height. There are inhabitants of lowland forests, of upland bogs, and of rocky cliffs. There are species producing fruit as dry capsules; others produce fleshy berries. So varied are the Hawaiian lobeliads that previous authors have inferred their origin from multiple seperate colonisations, but a study by Givnish et al. (2009) supported a single origin from a single colonist arriving about thirteen million years ago. This would have been before any of the current major Hawaiian islands existed (the oldest, Kaua'i, is a little less than five million years old); the implication is that the ancestor of the Hawaiian lobeliad arrived on a pre-existing island, perhaps corresponding to the modern Gardner Pinnacles or French Frigate Shoals. As the lobeliads diversified, they continued to disperse onto new islands as they arrived, while their original homeland eroded away.

Sadly, a depressing percentage of the species forming this incredible radiation are now threatened with extinction, the victims of pressures such as loss of habitat, the decline of their pollinators and dispersers, or grazing by introduced mammals. The cliff-dwelling pua 'ala Brighamia rockii of Moloka'i is now restricted to five locations with an estimated total wild population of less than 200 individuals. A related species on Kaua'i, the olulu Brighamia insignis, may be extinct in the wild, having last been recorded in the form of a single individual in 2014 (it still survives in cultivation). As we earlier saw with the Hawaiian honeycreepers, there is barely a single section of the Hawaiian biota not marked by tragedy.


Crowl, A. A., N. W. Miles, C. J. Visger, K. Hansen, T. Ayers, R. Haberle & N. Cellinese. 2016. A global perspective on Campanulaceae: biogeographic, genomic, and floral evolution. American Journal of Botany 103 (2): 233–245.

Givnish, T. J., K. C. Millam, A. R. Mast, T. B. Paterson, T. J. Theim, A. L. Hipp, J. M. Henss, J. F. Smith, K. R. Wood & K. J. Sytsma. 2009. Origin, adaptive radiation and diversification of the Hawaiian lobeliads (Asterales: Campanulaceae). Proceedings of the Royal Society of London Series B—Biological Sciences 276: 407–416.

Knox, E. B. 2014. The dynamic history of plastid genomes in the Campanulaceae sensu lato is unique among angiosperms. Proceedings of the National Academy of Sciences of the USA 111 (30): 11097–11102.


It's a general rule with organisms that species diversity increases as size decreases (at least down to about the millimetre range, below which things get a bit more complicated). That's certainly the case with molluscs, whose range clearly favours the tiny.

Alvania cimex, copyright Alboran Shells.

Alvania is a cosmopolitan genus of marine gastropods, found in most parts of the world except the Antarctic and sub-Antarctic (Ponder 1984). The average Alvania species is less than five millimetres in total length, and other members of the family they belong to, the Rissoidae, are similarly wee. The shell of Alvania species varies from elongate-conical to more squatly conical in shape, and generally has a sculpture of both axial and spiral ridges. In some species the axial and spiral ribs are both similarly prominent; in others, the spiral ridges are more strongly developed.

Rissoids may be found crawling on seaweed or sheltered amongst stones or other rubble. Alvania species seem to be more likely to be found in the latter habitat than the former. Alvania have a smaller mucous gland on the rear of the foot than species of Rissoa, a related genus that is more likely to be found on the weeds. The mucus produced by this gland assists rissoids in clinging to their substrate or the surface film, and its reduction in Alvania is presumably connected to their preference for the low life. Rissoids are grazers on microalgae or deposit feeders; those species found on seaweeds will feed on diatoms and the like growing over the seaweed rather than on the seaweed itself. Among European species, A. punctura is known to selectively pick out diatoms and dinoflagellates from among detritus when feeding whereas A. jeffreysi may be less discriminating in what it swallows.

Alvania subcalathus, copyright H. Zell.

The greater number of Alvania species are planktotrophic as larvae, and as described in some of my previous posts on turrids, their shells have protoconches to match. Nevertheless, the genus also includes some direct-developing species with fewer protoconch spirals. The Mediterranean species A. cimex and A. mammillata are almost indistinguishable when mature except by features of the shell apex, which is broader with fewer spirals to the protoconch in the latter (Verduin 1986). If A. mammillata is a direct developer while A. cimex has a planktotrophic larva, it would tally up with the situation elsewhere seen among turrids.


Ponder, W. F. 1984. A review of the genera of the Rissoidae (Mollusca: Mesogastropoda: Rissoacea). Records of the Australian Museum Supplement 4: 1–221.

Verduin, A. 1986. Alvania cimex (L.) s.l. (Gastropoda, Prosobranchia), an aggregate species. Basteria 50: 25–32.


I've commented before on the unexpectedly high diversity of animal species that can be found living in groundwater. Because dispersal through this habitat is, unsurprisingly, often difficult and bodies of groundwater are often isolated from each other, many groundwater-adapted species can have almost ludicrously small ranges. Hence, for instance, the diversity of the amphipod genus Niphargus.

Niphargus hadzii, copyright B. Sket.

The genus Niphargus is found across Europe, mostly south of what was the lower edge of the northern ice sheet during the Pleistocene, though it is replaced by a closely related genus in the Iberian Peninsula. A few species are also found in south-west Asia. They are usually eyeless and colourless (the genus name means 'snowy white'). Though clearly adapted for subterranean environments, they may also be found in associated surface habitats such as springs or the upper sections of streams (Fišer et al. 2015). Species of Niphargus vary considerably in size: the smallest interstitial species may be only two or three millimetres in length whereas some cave-dwellers reach forty millimetres (Karaman & Ruffo 1986). They may feed on organic particles filtered from the water, or they may predate on smaller animals.

Over 300 species of Niphargus are currently recognised, making it one of the largest genera of freshwater amphipods. Even so, this number is likely to be a significant underestimate of the genus' true diversity. A number of studies on Niphargus have identified evidence of previously cryptic species. A study by Fišer et al. (2015) of two species from the Istrian Peninsula in the north-west Balkans found genetic evidence for the existence of two strongly divergent populations within each, with the two populations of 'N. krameri' being morphologically as well as genetically distinct. Flot et al. (2010) found evidence of four distinct lineages within 'N. ictus' of Italy's Frasassi caves, representing at least three independent colonisations of the cave system from external sources. At least two of these lineages are unique among amphipods in living in a symbiotic association with sulphide-oxidising bacteria of the genus Thiothrix, allowing them to survive in Frasassi's sulphide-rich waters.

Niphargus aquilex from the River Till, copyright Lee Knight.

With such a large genus, attempts have naturally been made to divide it into more manageable units. About a dozen species groups have been recognised on the basis of morphology, albeit some poorly defined. However, a molecular phylogenetic study of the genus by Fišer et al. (2008) identified none of these groups as monophyletic. Instead, they found a higher correlation of phylogeny with geography than morphology. The picture suggested is one of poor dispersers, re-evolving similar forms on multiple occasions as they diverge to exploit their secluded habitats as best they can.


Fišer, C., B. Sket & P. Trontelj. 2008. A phylogenetic perspective on 160 years of troubled taxonomy of Niphargus (Crustacea: Amphipoda). Zoologica Scripta 37 (6): 665–680.

Fišer, Ž., F. Altermatt, V. Zakšek, T. Knapič & C. Fišer. 2015. Morphologically cryptic amphipod species are "ecological clones" at regional but not at local scale: a case study of four Niphargus species. PLoS One 10 (7): e0134384.

Flot, J.-F., G. Wörheide & S. Dattagupta. 2010. Unsuspected diversity of Niphargus amphipods in the chemoautotrophic cave ecosystem of Frasassi, central Italy. BMC Evolutionary Biology 10: 171.

Karaman, G. S., & S. Ruffo. 1986. Amphipoda: Niphargus-group (Niphargidae sensu Bousfield, 1982). In: Botosaneanu, L. (ed.) Stygofauna Mundi: A Faunistic, Distributional, and Ecological Synthesis of the World Fauna inhabiting Subterranean Waters (including the Marine Interstitial) pp. 514–534. E. J. Brill/Dr W. Backhuys: Leiden.

Wasps that don't Give to a Fig

The strategies employed by flowering plants to draw in their pollinators are many and varied. Some have entered into exclusive partnerships, contriving methods by which their rewards are shared with a single animal species and hence presumably increasing the likelihood of that species visiting them. Once remarkable example of such a partnership is found among the figs. To the casual observer, fig trees might appear to never produce flowers. However, immature figs are in fact closed inflorescences called syconia with the flowers produced on the inside of the fig, never exposed to the outside world. The only way for pollinators to reach the fig flowers is through a tiny hole or ostiole at the fig's apex. This ostiole is used by the fig's pollinators, tiny female wasps of the chalcidoid family Agaonidae, who enter the fig in search of places to lay their eggs. The wasp herself does not leave the fig again after laying but her eggs and larvae develop within galls inside the fig, feeding on the tissue of the fig itself. After developing into wingless males and winged females, the next generation of fig wasps mates within the syconium; pollination of the fig tree occurs through the young females leaving the fig to find their own laying places and carrying pollen as they do so.

Female Idarnes nr flavicollis, a typical late-laying sycophagine, copyright Sergio Jansen Gonzalez.

The fig benefits by having an exclusive pollinator, the fig wasp benefits by having a ready-made nursery for its offspring. However, all that tasty fig tissue is bound to prove attractive to others who would circumvent the standard contract. Another group of chalcidoid wasps, the subfamily Sycophaginae, includes prime examples of such freeloaders. Like the true pollinating fig wasps, these non-pollinating fig wasps develop in galls within fig syconia. However, instead of entering the fig through the ostiole, most sycophagines use their ovipositor to pierce the fig's outer skin and lay from outside. In some sycophagines, the ovipositor is relatively short and thick; these species lay their eggs when the fig is only just beginning to develop. In others, the ovipositor is longer and slender, longer in fact than the rest of the wasp, and oviposition happens later when the fig has grown to a larger size. In some of these later-arriving forms, the ovipositing female lays into a gall already induced by the fig's actual pollinator (how she finds it from outside the fig, I have no idea), and as well as feeding on the gall, her larva will eventually feed on the pollinator larva. There are also some sycophagines that enter the syconium through the ostiole and oviposit internally; I haven't been able to find whether these species may function as true pollinators.

Female Sycophaga ovipositing on Ficus sur, copyright JMK.

As noted above, pollinating agaonids exhibit strong sexual dimorphism with only the females having wings, and males never escaping the host syconium. The wingless males cannot be easily recognised as belonging to the same species as the females; indeed, if one does not already know what they are, they can barely even be recognised as wasps. In sycophagines, matters are a bit more complicated. In some species, males are wingless and highly modified as in pollinating fig wasps. In others, males are winged and similar in appearance to females. And in still others, wingless and winged males are both present within a single species. I don't know what determines whether a given larva of these species develops wings or not; both forms may develop within the same syconium. It has been suggested that the presence of the two forms is related to conflicting pressures of gene flow vs speed. Winged males that can look for mates outside the parent syconium have a better chance of finding mates outside the pool of their own siblings, thus avoiding the risk of inbreeding. However, wingless males can mate with females immediately after they emerge within the syconium (if not before, as I'll explain shortly), in which case the winged males may simply find themselves too late to the party. Certainly there is a correlation between winglessness and the size of broods. Early-ovipositing species, which tend to produce smaller broods because the younger host syconium offers less space for egg-laying, are more likely to have winged males whereas males of later-ovipositing species are more likely to be wingless (Cruaud et al. 2011).

Male Apocryptophagus, copyright Centre for Biodiversity Genomics.

Males of the genera Sycophaga and Apocryptophagus (which Cruaud et al., 2011, suggested should probably be synonymised) are invariably wingless and have elongate, flattened, extensible gasters. The terminal pair of spiracles on the abdomen have the surrounding peritremes (supporting rings) extended into a pair of long filaments. In the host figs of these genera, the interior of the syconium becomes filled with liquid after being pollinated by its associated agaonids; the liquid is resorbed when the pollinators emerge. Nevertheless, there are advantages for the sycophagines in emerging before the pollinators: not only could the interior of the syconium become rather crowded, males of some agaonid species have enlarged mandibles that they may use to dispatch any interlopers. So instead of waiting for the syconial fluid to drain away, the male Sycophaga cuts a small opening slit in his gall (too narrow for the surrounding fluid to seep in) through which he partially emerges into the central cavity. The peritremal filaments are used to anchor the end of his gaster within his original gall so that he can continue to breathe from the air-pocket inside it while he stretches out in search of another gall containing a female. When he finds one, he will cut into it in the same way that he cut out of his own, then release the end of his gaster from its anchor-point and quickly slip into the gall of his intended. After a brief mating, he can repeat the process, this time using the female's gall as his air-tank (Ramírez 1996–1997). The female presumably emerges once the syconial fluid is gone.

Male Apocryptophagus emerging from a gall containing a female, from Ramírez (1996–1997).

There have been various viewpoints about the relationships of Sycophaginae to other chalcidoids. Some authors have included almost all the fig-associated wasps in the Agaonidae, whether pollinators or not. Others have restricted the Agaonidae to the true pollinators and classified non-pollinating fig wasps such as the Sycophaginae with the poorly defined family Pteromalidae. An analysis of chalcidoid relationships by Heraty et al. (2013) identified Sycophaginae as a sister group to Agaonidae sensu stricto (while placing other groups of non-pollinating fig wasps elsewhere on the tree). This might lead one to consider the possibility that the gall-making habit seen in both Sycophaginae and pollinating Agaonidae pre-dates the evolution of the wasp-fig relationship as pollinators. Perhaps the evolution of the syconium allowed figs to convert gall-makers that had previously been parasites into partners.


Cruaud, A., R. Jabbour-Zahab, G. Genson, F. Kjellberg, N. Kobmoo, S. van Noort, Yang D.-R., Peng Y.-Q., R. Ubaidillah, P. E. Hanson, O. Santos-Mattos, F. H. A. Farache, R. A. S. Pereira, C. Kerdelhué & J.-Y. Rasplus. 2011. Phylogeny and evolution of life-history strategies in the Sycophaginae non-pollinating fig wasps (Hymenoptera, Chalcidoidea). BMC Evolutionary Biology 11: 178.

Ramírez, W. 1996–1997. Breathing adaptations of males in fig gall flowers (Hymenoptera: Agaonidae). Revista de Biologia Tropical 44 (3)–45 (1): 277–282.