the new zealand flax snail or pupuharakeke , scientific name placostylus bollonsi , is a species of air-breathing land snail , a terrestrial pulmonate gastropod mollusc in the family bothriembryontidae .

this species is endemic to the three kings islands group off the northern tip of new zealand 's north island .

new zealand flax snail

the new zealand flax snail is found in the north island of new zealand . these land molluscs eat leaves from trees such as karaka and the kohekohe . despite their name they do not eat flax . new zealand flax snails live under broadleaf forests and other vegetation .
far northern new zealand in the pliocene , 10 million years ago , was a series of islands , and it is considered that the three new zealand species of placostylus developed on these .
how to cite this page : ' snail , flax or pupuharakeke ' , from an encyclopaedia of new zealand , edited by a . h . mclintock , originally published in 1966 . te ara - the encyclopedia of new zealand url : urltoken ( accessed 10 jul 2018 )
find out about new zealand biodiversity inventory and monitoring research projects , conducted by doc and other organisations .
flax snails / pupurangi ( placostylus spp . ) belong to the group of northern giant land snails , which contain some of new zealand ' s largest snails .
this species is endemic to new zealand , where it almost certainly occurs at only five locations ( powell 1979 ) .
parrish , r . , stringer , i . , sherley , g . and gleeson , d . management - related research on new zealand flax snails ( december , 2006 ) urltoken
parrish , r . , stringer , i . , sherley , g . and gleeson , d . management - related research on new zealand flax snails ( october , 2006 ) urltoken
confined to the te paki ecological region in the far north of northland , new zealand ( 2 ) ( 6 ) .
hayward , b . w . and brook , f . j . ( 1981 ) exploitation and redistribution of flax snail ( placostylus ) by the prehistoric maori . new zealand journal of ecology , 4 : 33 - 36 .
flax snails belong to the worlds oldest land snail family witch originated 200 to 300 million years ago .
this draft strategy sets out the new zealand government’s plan to halt the decline in our threatened species and restore them to healthy populations .
documents relevant to the management of the lord howe flax snail can be found at the start of the profile .
sherley , g . ( 1994 ) . translocations of the mahoenui giant weta deinacrida n . sp . and placostylus land snails in new zealand : what we have learnt ? . in : reintroduction biology of australian and new zealand fauna . serena , m : 57 - 63 . surrey beatty and sons , chipping norton , new south wales .
flax snails ( placostylus spp . ) are endemic to new zealand and belong to the world’s oldest land snail family , which originated 200 to 300 million years ago ( 3 ) . the long , coiled , shiny brown shell of this particular flax snail species can reach up to an impressive 9 . 4 centimetres ( 2 ) ( 4 ) . sadly , the beauty of their shells was fatal for many flax snail species , before shell collecting became illegal in 1982 ( 5 ) .
brook , f . j . and mcardle , b . h . ( 1999 ) morphological variation and biogeography of placostylus hongii ( gastropoda : bulimulidae ) , northern new zealand . journal of the royal society of new zealand , 29 ( 4 ) : 407 - 434 . available at : urltoken
flax snails usually live in broadleaf forest and scrub . growing as big as 115 mm , flax snails / pupurangi are not your average garden snails . t
this flax snail is on a branch on the mokohinau islands . snail hatchlings spend an unknown period living in trees and shrubs , then move down on to the forest floor .
the lord howe flax snail is believed to feed on the fallen dead leaves of broadleaf trees ( ponder & chapman 1999 ) .
another ancient group of large snails is represented locally by the flax snails placostylus .
new south wales national parks and wildlife service ( nsw npws ) ( 2001a ) . lord howe placostylus placostylus bivaricosus ( gaskoin 1855 ) recovery plan . hurstville , new south wales : new south wales national parks and wildlife service .
this information was published in 1966 in an encyclopaedia of new zealand , edited by a . h . mclintock . it has not been corrected and will not be updated .
colourful tree snails are common in the islands , whereas new zealand has no true tree snails . there are also fewer small species than in new zealand , but more larger ones , though there is nothing to compare with the magnificence of our powelliphanta .
paryphantidae are not the only members of this ancient club . a number of elements of the new zealand fauna—frogs , lizards and other land snails—all suggest that new zealand has been isolated from other land masses for the last 60 million years and possibly longer .
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like other large flax snails , this species has been badly affected by mammalian predators introduced to new zealand , such as rodents , pigs , hedgehogs and possums ( 8 ) . habitat destruction and modification wrought by human settlers and the domestic and feral animals they brought , such as sheep , cattle , horses , goats and pigs , which graze , browse and trample vegetation , has also had a dramatic and devastating impact on flax snail numbers ( 2 ) ( 8 ) . these threats continue to grow and , without intervention , could lead to the extinction of one of new zealand’s largest native snails ( 8 ) .
scientific name : placostylus bivaricosus . common name : lord howe flax snail . other names : lord howe placostylus . three subspecies of the lord howe flax snail are currently recognised on the basis of shell morphology ( australian museum 2001 ) ; placostylus bivaricosus bivaricosus , p . bivaricosus cuniculinsulae and p . bivaricosus etheridgei .
management of the main flax snail colonies has existed since the early 1980s , mostly through poisoning rodent predators , enhancement planting , fencing colonies and stock control ( 2 ) . shell collecting became illegal in 1982 ( 5 ) , and all placostylus species have the status of nationally threatened invertebrates , and as such are protected and intensively studied by the new zealand department of conservation ( 4 ) . new zealand’s department of conservation also created a giant land snail recovery plan in 1995 , which has since been updated , and aims to prevent extinction and focus management towards the most genetically diverse populations ( 2 ) .
parrish , r . , g . sherley & m . aviss ( 1995 ) . giant land snail recovery plan placostylus spp . , paraphanta sp . threatened species recovery plan series no . 13 . new zealand : threatened species unit , department of conservation .
although helix aspersa , the common garden snail , and its many pestiferous slug cousins are european immigrants , new zealand is well endowed with its own native snail fauna , plus a sprinkling of slugs . these natives spurn agricultural delicacies , far preferring the dank underworld of the forest floor , and it is likely that most new zealanders have never seen a single one , although we may have as many as 1000 species .
the total population of the lord howe flax snail is estimated to be less than 1000 mature individuals . the abundance of dead snail shells provide an indication of the historical widespread abundance of the lord howe flax snail in the mid - island lowlands . in some areas , shells occur in densities of up to 30 shells / m² in many parts of the settlement area ( ponder & chapman 1999 ) .
they eat leaves from trees such as karaka , kohekohe and rangiora despite there name they dont eat flax .
the age of sexual maturity and lifespan of the lord howe flax snail are unclear , but related placostylus species in new zealand reach sexual maturity at three to five years and may live for 20 years or more ( parrish et al . 1995 ) . the lord howe flax snail lays small clutches of round eggs in the soil beneath leaf litter , probably during late spring and summer . the eggs hatch into small - shelled snails about 7 mm in length and 5 mm in width . hatchling and juvenile mortality is high ( ponder & chapman 1999 ) .
this flax snail is recorded from new zealand’s mainland at sites between whangaroa and whangarei on the northland coast , and from the poor knights , chicken , mokohinau and great barrier islands offshore . however , a number of populations are now extinct or believed to be extinct ( 6 ) . recently translocated populations are also present on motuhoropapa ( 6 ) and matakohe / limestone islands ( 7 ) .
management of priority flax snail colonies has been carried out since the early 1980s . most of this management has consisted of rodent control , enhancement planting , fencing colonies and stock control . these actions have successfully allowed some species of flax snails to recover from near extinction to colonies of some hundreds . research has also been conducted on different aspects of snail ecology .
new zealand has around 1000 species of native land snails , yet most people have probably never seen a single one . warren judd reveals something of the glory of these creatures and their shell - less relatives the slugs .
the lord howe flax snail is a large land snail . it has a pointed , conical shell up to 8 cm long , is medium to dark brown in colour ( weathering to white in older specimens ) and has a thickened lip in mature adults . the soft body parts are black ( new south wales national parks and wildlife service 2006 ) .
like other large flax snails , this species has been badly affected by mammalian predators introduced to new zealand , such as rodents , pigs , hedgehogs and possums ( 6 ) . habitat destruction and modification wrought by human settlers and the domestic and feral animals they brought has also had a dramatic and devastating impact on flax snail numbers , with sheep , cattle , horses , goats and pigs grazing , browsing and trampling vegetation ( 2 ) ( 6 ) . as a result , this species , like many other flax snails , now survives only in a small reserve where it is protected and where the predators are controlled ( 4 ) .
parrish , r . , sherley , g . and aviss , m . ( 1995 ) giant land snail recovery plan placostylu spp . , paryphanta sp . – threatened species recovery plan series no . 13 . department of conservation , threatened species unit , wellington , new zealand . available at : urltoken
parrish , r . , sherley , g . and aviss , m . ( 1995 ) giant land snail recovery plan placostylu spp . , paryphanta sp . – threatened species recovery plan series no . 13 . department of conservation , threatened species unit , wellington , new zealand . available at : urltoken
a different species of these type of snails live in new caledonia where locals eat them as a delicacy .
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ponder , w . & r . chapman ( 1999 ) . survey of the land snail placostylus bivaricosus on lord howe island . unpublished report to new south wales national parks and wildlife service .
sherley , g . , i . a . n . stringer , g . r . parrish & i . flux ( 1998 ) . demography of two land snail populations ( placostylus ambagiosus , pulmonata , bulimulidae ) in relation to predator control in the far north of new zealand . biological conservation . 84 : 83 - 88 .
flax snails usually live in broadleaf forest and scrub . they reside in pockets of broadleaf litter , or under ground cover vegetation .
the placostylus snails are significant in the reconstruction of former land connections , for they occur outside new zealand only in the melanesian islands , northwards to the solomons , and eastwards to fiji . this area of distribution coincides with the now largely submerged “melanesian plateau” .
will you walk a little faster ? ” said a whiting to a snail .
mating in flax snails appears to be triggered by rainfall and probably occurs every year , except in periods of drought . these snails may mate several times with several different partners . in a different flax snail species , egg - laying has been observed between november and february , with 20 to 30 eggs laid in a shallow nest in loose earth . nests containing 30 or more eggs are thought to be the result of more than one snail laying in the same nest ( 6 ) . while adult flax snails tend to stay in and around a relatively small area , the juveniles disperse widely ( 7 ) . these flax snails reach maturity at three to five years of age and may live for over 20 years ( 6 ) .
a captive breeding program for the lord howe flax snail has commenced , which engages the help of the local school on lord howe island . the program involves the construction of a number of rat - proof pens , which are provided with shade and appropriate leaf litter , in which breeding populations of the lord howe flax snail may be established and maintained . adult snails reared in the program are released back into natural populations to maintain genetic diversity ( ponder & chapman 1999 ) .
endemic to new zealand , flax snails ( placostylus spp . ) belong to the world’s oldest land snail family , which originated 200 to 300 million years ago ( 3 ) . the long , coiled brown shell of this large snail species can reach enormous lengths of more than eight centimetres ( 2 ) ( 4 ) . some populations contain albinos , which are characterised by a white to pale - yellow rather than bright orange or red colour within the shell opening ( aperture ) . the outside of the shell ( periostracum ) is also paler brown in some albinos , but the shells of the two forms otherwise appear identical ( 5 ) .
new zealand has other interesting genera of snails in the paryphantid family besides powelliphanta . in northland , paryphanta busbyi , the kauri snail ( termed pupurangi or whistling snail by the maori ) is still common in places , and human intervention has re - established it in other areas , such as auckland’s waitakere ranges . this snail has a black animal inhabiting a dark greenish shell 45mm in diameter . the colour resides in an exterior proteinaceous periostracum made of conchin , and this overlies a fairly solid calcareous shell . shell structure in powelliphanta is similar , but the calcareous layer is much thinner .
control rodents , as they prey on juvenile snails . snail populations greatly benefit from rodent control .
norman gardner , a retired cabinet maker in birkenhead , auckland , was perhaps the first of the scientific amateurs to become really interested in snails , and he has been pursuing them for close to 50 years . although still very active in snail work , he has followed a somewhat different trajectory . in recent years he has left new zealand snails to others and concentrated on the many neglected pacific island species .
flax snails generally inhabit coastal broadleaf forest and scrub , residing in pockets of leaf - litter on the ground ( 2 ) ( 4 ) . young flax snails live on the leaves in the tree canopy , only coming to live on the ground when they have grown sufficiently large ( 4 ) ( 6 ) .
flax snails generally inhabit coastal broadleaf forest and scrub , residing in pockets of leaf - litter on the ground ( 2 ) ( 4 ) . young flax snails live on the leaves in the tree canopy , only coming to live on the ground when they have grown sufficiently large ( 4 ) ( 8 ) .
snail hatchlings spend an unknown period living in trees and shrubs up to 6 metres above the ground .
the periodic use of the biodegradable poison 1080 to kill possums has reversed the decline in snail populations .
snail farmer hans pos has seen snails with uncoiled shells , where the seams have not sealed up .
although this sounds fairly reasonable , in some of frank’s recent writing panbiogeography seems to burst out from the prosaic manacles of snail taxonomy to recast the world . in the new zealand journal of zoology frank writes : “panbiogeography will remove much fear … . from the international community . this reduction in fear levels ( a measure of the reducing power of the collective unconscious ) will improve international relations , make rabid ‘nationalism’ irrelevant and thus make humanity more healthy . ”
and how’s this for a new agricultural twist ? snail eggs . hans tells me that in europe people regard them as a health food delicacy , and they fetch the same price as caviar—around $ 50 per 50 grams . “you can buy them in harrods , ” says hans .
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control pigs . they are also a predator , and eat adult snails as well as damaging snail habitat through rooting .
such ages place powelliphanta amongst the methuselahs of the snail universe , where lifespans of 1 - 5 years are common .
adult lord howe flax snails are readily identifiable due to their large size and pointed , conical shell . however , juvenile snails may be easily confused with other species and generally require expert identification .
lord howe placostylus placostylus bivaricus ( gaskoin , 1855 ) recovery plan ( new south wales national parks and wildlife service ( nsw npws ) , 2001b ) [ state recovery plan ] .
in new caledonia a major predator on plactostylus is man . new zealanders , being a gastronomically cautious lot , largely eschew snails . of course , the mercurial french are renowned for their penchant for escargots . afficionados assure me that , laced with garlic sauce and olive oil , snails are great . and the opportunity exists to try snails locally ( though not placostylus ! )
the main food plants are karaka , kohekohe , coprosma , rangiora , planchonella and lace bark—all coastal broadleaf species . pohutukawa , flax , five finger and taraire provide shelter only , and are not eaten .
the first department of conservation giant land snail recovery plan was approved in 1995 and is currently being updated . the new plan sets in place a series of steps that will promote the recovery of the snails . it also outlines different management options and a work plan . the long - term goal of this recovery plan is :
for those who relish the thought of “getting their own back” by eating the snails that demolished their plants , we present the following notes on the preparation of the common garden snail helix aspersa for the table , courtesy of hans pos , snail farmer and consultant .
the two populations of the lord howe flax snail are included in permanent park preserve and environment protection areas ( lord howe island board 1986 ) . however , the majority of recent records are outside the island ' s formal reserve system , with many occurring in the settlement area where they may be at risk from development ( nsw npws 2001a ) .
a far greater range of species can be found in auckland’s waitakere ranges . jim goulstone , a knowledgeable snail enthusiast and a professional tomato grower , has compiled a checklist of 120 species found in the waitakeres . an extra 30 species occur in other bush areas in the greater auckland area . many have a surprisingly narrow distribution . “you would expect there to be north - south differences in snail distribution in new zealand , ” explains jim , “and there are some , but there are also marked east - west differences , even when the country is as narrow as it is around auckland . quite a few extra species can be uncovered in the hunuas that aren’t present in the waitakeres . ”
curtis , h . s . ( 1998a ) . snail collection - lord howe island . unpublished report to lord howe island board .
these collectors are a vital part of the scientific process and are experts in their own right . most have discovered new species of snails , and some have been rewarded by having species named after them .
place a little garlic butter into each shell , replace the snail , and pack more butter mix around it until the shell is full .
australian museum ( 2001 ) . threatened and endangered land snail species . page ( s ) 2001 . australian museum invertebrate zoology internet site .
p . bivaricosus etheridgei has declined in range and abundance . it may survive as a number of small , isolated local populations , based on the identification of hatchling snails collected from leaf litter in the 1970s ( ponder & chapman 1999 ) . given the persistent threats to the species , it is suspected the lord howe flax snail will continue to undergo a reduction in numbers .
anne strachan , who kept powelliphanta for several years , noted peculiarities in the snails’ eating behaviour . “it seemed to me that the snails put out a substance that affected the worms when they wanted to feed , ” she told me . “usually the worms crawl over the snail’s mucus trails no trouble at all , but when the snail is hungry , the worm blanches and goes limp as soon as it touches snail mucus . ”
if you are a slug or snail , just getting around uses up a lot of water—it’s almost a fuel . mucus , that silver trail snails leave , is essential in locomotion , and water is its main constituent . prevent the snail secreting mucus and it can’t move . although all snail mucus seems glutinous and clinging , it apparently has different properties depending on whether it’s on the back of the animal , in the gut or lubricating the sole of the foot .
the minute new zealand species are also more notable for architectural exuberance . sculptural detail of such delicacy that it requires a scanning electron microscope to unlock its intricacies is common . some species are tall spired , others flat , and every conceivable intermediate form exists . some resemble beehives while others compensate for more pedestrian form with elaborate surface plates , giving them the appearance of mini - turbines . hairs and bristles cover the surface of many species , and yet others sport complex arrays of plates in their apertures .
kath has set up snail houses in the grounds of several homes she has occupied and after a lot of tedious work in providing the moisture , humidity , calcium and food they need , has succeeded in growing and breeding powelliphanta , making many unique and fascinating observations along the way . for instance , she recalls seeing two snails trying to eat the same worm . “one evening a medium - sized snail had almost completely ingested a big worm when a larger snail latched onto the other end . next morning , both snails were still mouth to mouth , tugging at the worm , but the bigger snail finally got it all . ”
“they buried this sole live specimen in the flax , ” she recalls , “but eventually decided it was doomed to become rat fodder , so noman reluctantly brought it home to waiuku . there it laid fertile eggs for three and a half years , and he was eventually able to return a number of individuals to the wild . ”
despite frank’s somewhat unorthodox ideas on panbiogeography and snails as the key to the cosmos , he does know a lot about these creatures . his special interest is the myriad species of small snails found throughout new zealand . the largest of them would be the size of the extinct one cent piece , but most are much smaller , and plenty are no larger than a pinhead . shy and retiring , they are the sort of thing that you rarely find unless you are looking for them , and not too many people grub in the dark heaps of decaying leaves and wood favoured by the snails . even then , it takes a trained eye to spot them .
according to kath , powelliphanta lay one or two eggs per week during the spring , and they are huge compared to the size of the snail . shaped like birds’ eggs , the largest are 12 - 14mm long—not much smaller than a sparrow’s egg ! eggs are laid in the ground ( from an aperture near the mouth , not the rear end ) and require 2 - 9 months to hatch out a young snail .
powelliphanta lignaria rotella was just one subspecies that was largely exterminated by these endeavours . the department of conservation has ironically now been presented with some of this mutilated snail habitat ( unlike the wildlife service , doc has responsibilities for habitat ) and has considered felling the young exotics , reflattening the land and replanting native trees ! frank climo is right . the snail’s spirality does capture that clearsighted , unflinching directness we associate with public administration .
placostylus bivaricosus ( a large land snail ) - endangered species listing . nsw scientific committee - final determination ( nsw department of environment , climate change and water ( nsw deccw ) , 1997e ) [ internet ] .
a few years back retired agricultural consultant hans pos encouraged school children to collect the common introduced helix aspersa . with promises of a new export industry catering to discerning european palates . unfortunately , the venture never really prospered , but there are a few people farming snails locally and supplementing their incomes by selling them to restaurants .
this is a tall - spired , solidly built chocolate to reddish - brown land snail up to 3 in . in height . formerly these snails were abundant along the northland east coast from whangarei to whangaroa , but , with the clearing of coastal forest , they now exist only in a few isolated spots . the species , however , still survives in strength at the poor knights islands . these snails are vegetarian and feed largely upon fallen karaka leaves . they are found hidden under leaves and around sedges , but in flax only when there is no other cover .
but what of the snail eggs , a delicacy highly regarded in europe — can the connoisseur prepare his own ? unfortunately , the recipe is a commercial secret , but some clues can be gleaned from a producer’s brochure .
one of the most bizarre stories concerns achatina fulica , the giant east african snail . this beauty reaches 200mm in length , grows at a prodigious rate and can survive in most tropical and subtropical climates . it has become undisputed winner of the title “world’s most dreaded snail” . man is the agent by which it has spread—from fascinated aristocrats taking it home , to eggs carried on tank tracks during world war ii . many tourists have taken home shells ( sometimes even painted ones ) certain that they were empty , when in reality the snail was just biding its time . a few years later , abundant progeny of the neglected souvenir wreak devastation on ornamental and agricultural plants .
when designing his snail characters , silver at first attempted to give them eyes in the proper places—on the end of their tentacles . “but they looked like creatures from outer space . so i gave them eyes on their heads . ”
the brown shells bear more than a passing resemblance to the dead leaves in which they live and feed . snails are active only on wet nights , which means they spend a lot of time resting . by marking individuals , andrew discovered that they do not range more than five metres in a year , and many will still be under the same flax bush they were placed in 12 months earlier !
the whiting’s words capture what most of us think about snails : a synonym for excruciatingly slow . but how fast do they really move ? big slugs can cover 15cm per minute ( a kilometre in 4 - 5 days ) , the garden snail manages 7 . 5cm / min , with small snails clocking in at at sl , iggish lcm / min a costa rican mountain snail holds the record : 45cm per minute . this speedster lifts the front of its foot off the ground to reduce drag !
mating appears to be triggered by rainfall and probably occurs every year , except in periods of drought . these snails may mate several times with several different partners . egg - laying has been observed between november and february on poor knights , when 20 to 30 eggs are laid in a shallow nest in loose earth . nests containing 30 or more eggs are thought to be the result of more than one snail laying in the same nest ( 8 ) . while adults tend to stay in and around a relatively small area , juveniles disperse ( 9 ) . these flax snails reach maturity at three to five years of age and may live to over 20 years ( 8 ) .
like many longer - lived animals , powelliphanta lays a small number of large eggs . although hermaphrodites , powelliphanta usually mate and fertilise each other . mating involves one snail sitting on top of another and the two exchanging sperm packets . it is accompanied by a lot of bubbles .
brazier ( 1889 ) noted that the lord howe flax snail was abundant under cover in shady , damp situations and on scrubby calcarenite ( chalky ) hillsides , was sparingly represented at higher altitudes and appeared to avoid open areas . ponder & chapman ( 1999 ) found the species sheltering under leaf litter in forest often , but not exclusively , in the vicinity of banyan trees ( ficus columnaris ) and mostly on calcarenite - derived soils and sandy soils . the vegetation at all sites where recent observations have been made is either kentia palm ( howea fosteriana ) closed - forest or greybark ( drypetes australasica ) - blackbutt ( cryptocarya triplinervis ) closed - forest or a combination of the two ( curtis 1998 ; pickard 1983 ; ponder & chapman 1999 ) .
local snail farmers use brassicas for food and can carry up to 150 snails per square metre , or 1 . 5 million per hectare . ( eat your heart out , sheep farmers , where 10 per hectare is about average ! ) above 150 per square metre everything becomes covered with slime .
however , while a human’s blood circulates in only 21 seconds , a snail’s takes six minutes ! but don’t be smug ; snails have blue blood . the oxygen - carrying pigment is copper - based haemocyanin , rather that the iron - containing haemoglobin of humans . when charged with oxygen , the blood is sky blue , but deoxygenated in the veins it is almost colourless . over one third of the weight of a slug is thought to be blood , whereas in humans blood is less than 10 per cent of the body weight . unlike mammalian blood , snail blood does not clot .
serve the stuffed snails on special snail plates or else use an apple corer to cut nine holes in thick slices of bread . place the slices on a buttered baking dish and insert the snails into the holes . prior to serving , place the dish in an oven preheated to 220 ° c .
apart from the eggs , snail meat is being increasingly sought as a food . the traditional french fare is helix pomatia ( a bit bigger than h . aspersa ) , although h . asperse , the “little grey” , is also popular . demand is outstripping orthodox supply , resulting in exploitation of alternative species .
in some parts of the world achatina has actually made agriculture impossible . in florida , a state of emergency was declared when the snail was discovered in 1969 . using all the powers of the state , it still took four years to eliminate 18 , 000 snails and eggs from just a few infested kilometres .
the mating habits of our 20 or 30 native slugs are unknown . these species occur mostly in the south island , and all belong to one distinctive group . they bear a close resemblance to a slender four - centimetrelong dead leaf of yellowish hue with darker veins . the slime they exude has a distinct yellow tinge . a few species have the eyes on short stalks , but there are no other tentacles . some favour damp leaves or rotting wood while others prefer the closeness of flax and nikau palm leaf bases .
the shells look perpetually secure , but apparently not so . most small land snail shells are precariously fragile—mainly protein with little calcium carbonate . leaf litter tends to be acidic , and thin calcium shells would be in danger of being dissolved by acid . a protein skin on the shell—termed a periostracumprotects the shell from this hazard .
it seems that fertilisation does not always require two individuals . kath walker kept a solitary powelliphanta in monastic confinement for 18 months , and this individual eventually produced fertile eggs , suggesting that snails may self - fertilise if necessary . ( some doubt remains , because snails can store viable sperm from another snail for long periods . )
perhaps this relaxed pace of living is responsible for the snail’s longevity : it is suspected that individuals live for at least 10 years . provided they escape predators . rhvtida and paryphanta probably eat young placostylus , and on the poor knights an unexpected predator is the large shore crab leptograpsus , which can crush the spire of the shell with its pincers .
although snails are no sprinters , they can climb vertically and even upside down without slowing down . this is entirely due to the viscosity of the mucus produced by the pedal gland , near the front of the sole of the foot . often a snail will fall off a steep incline when first placed there because it takes a few seconds to produce enough of this pedal mucus to attach the animal the cells in the skin which covers the foot also produce mucus , but it is more watery in consistency and does not appear to assist adherence and locomotion . in some species additional mucus originates from a gland near the posterior end of the foot and this mucus is consumed by the snail’s partner during mating .
rhytida is a genus containing smaller dull - brown calcareous - shelled paryphantids which are cannibalistic . the shell of wainuia resembles a small , completely decalcified paryphanta . it is very fragile and translucent when empty . murray efford of ecology division , dsir , has recently observed those snails feeding on amphipods ( sandhopper types ) —the first snail found to prey on live arthropods anywhere .
the department of conservation is not the only body interested in the well - being of placostylus . s . o . s . ( save our snails ) was started in auckland nine years ago and is dedicated to “protecting and promoting endangered invertebrates , ” according to andrew jeffs , one of the founders . the organisation has made several attempts to safeguard placostylus populations , including laying rat poison in the worst affected colonies at either end of spirits bay and around cape maria . seeds and cuttings of snail food plants in the far north were raised to plantable size in auckland and then replanted to improve habitat and food supply in snail colonies . sos members even fenced a steep hillside above spirits bay to protect a couple of hectares of snails from larger animals .
each individual snail usually has both male and female reproductive organs , so they are true hermaphrodites . the reproductive system is elaborate , and its details are used to separate one species from another . snails also possess sophisticated digestive , circulatory , nervous , excretory and locomotory systems . surprisingly for such complex animals , they seem able to regenerate all body parts except the central nervous system .
slugs are really just land snails without shells , but many still possess internal shell rudiments . a few snail species seem to be halfway between slugs and snails , with shells still clearly visible but reduced to fig - leaf proportions . members of the genus schizoglossa are one such group . the shell looks like that of a 15mm paua , but provides meagre protection for the 50mm animal .
three small related snail species in the negev subsist on a lichen that bores into limestone rock . in getting at the lichen , the snails grind away the rock with their radulas , turning 100 grams of rock into dust each year in every square metre of desert . their faeces supply a significant amount of nitrogen to desert shrubs , so snails there are helping the desert to blossom .
as with most animals , snails and slugs have their abnormalities . the majority of snail shells coil to the right . however , a few left - handed shells turn up . dr a . w . b . powell noted that one of the first specimens of placostylus hongii he found was such a variant , but in all his years of study and collection he never found another .
in the circulatory department , snails possess arteries , veins , capillaries and a heart—complete with auricle and ventricle . data on pulse rate is scanty , but suggests 40 - 90 beats per minute is healthy . bigger specimens have slower pulses . while the snail’s blood output from the in the circulatory department , snails possess arteries , veins , capillaries and a heart—complete with auricle and ventricle . data on pulse rate is scanty , but suggests 40 - 90 beats per minute is healthy . bigger specimens have slower pulses . while the snail’s blood output from the heart is 5m1 per 100g body weight per minute , in man it is only 6 - 10m1 ! the total work performed by the heart is only 10 per cent higher in humans than in snails , when calculated on a weight basis .
norm gardner was interested in placostylus as long ago as the mid - 1940s . “even then they were not abundant , ” he says . “major predators were ( and still are ) rats and pigs . wild pigs are especially devastating in that they root right into the bases of flax bushes where the snails often hide . as well as eating snails , the pigs destroy their habitat . wild cattle also roamed over the entire area , trampling snails and damaging habitat . since roads were improved in the far north in the early 1970s , thousands of visitors have flocked into the area over summer , and these haven’t done anything for the snails . ”
powelliphanta are not exactly outgoing . at times photographer michael schneider and i crouched for four or five hours vainly waiting for snails to emerge from their shells . and if they were coy about public appearances , eating in front of humans must have been the ultimate breach of snail etiquette . pushing enormous worms into their faces elicited not the slightest interest ( though later michael was successful with garden worms . )
snails do , however , make other contributions to human society . engineers continue to be inspired and challenged by the shells not just of land snails but of all molluscs . the essence of concrete is cement ( calcium carbonate ) which is the main component of a shell . how is it that the strength to weight ratio of a shell is so superior to man - made concrete ? the answer proves to be partly in the long protein fibres mixed in with the calcium , and this is inspiring new forms of concrete containing glass or carbon fibres to produce stronger and lighter products . an australian experimenter has even made concrete microlight wings !
the stately snail has another message to teach us too , this about our past . it is hard to imagine the large buried eggs of these creatures being dispersed across seas by breezes or on the feet of wekas . despite kath walker finding a live powelliphanta washed up on a golden bay beach , it strains credibility to envisage these snails as powerful swimmers or even blithe windsurfers . they have been dispersed by measured crawling or tectonic movements ( which is faster ? ) .
the main human threat to these large snails has never been shell collectors , but habitat destruction . home for some of these snail varieties has frequently been a very restricted patch of bush . one type found at the tip of the west coast survives in only a hectare of very disturbed bush on a farm . among the worst affected snails have been those on the horowhenua plain , inhabiting diminishing bush remnants in a busy agricultural area where human activities have obliterated a number of colonies .
the functional significance of much of this sculpture is obscure , but one guess is that the sculpture stops dirt clinging to the shell . to a two - millimetre snail , even a speck of dirt could represent a sizeable bur den . longer shells ( 10mm - plus ) are much less elaborate . apertural plates perhaps serve to reduce water loss from the resting animal to a slimy , soft - bodied mollusc , living in air is hazardous . drying out is a constant danger , hence the damp habitats and nocturnal behaviour .
reproduction in snails and slugs is far from simple , either in physiology or behaviour . as well as being endowed with both male and female systems ( in most cases ) many pulmonates go to the trouble of manufacturing calcareous “love darts” which are some millimetres in length and which they “fire” at any potential partner that comes within range . the darts appear to function as a mating stimulus , but they frequently miss their target and are wasted . this must be a nuisance to the snail , for the darts take three or four days to manufacture .
“i’ve been interested in culturing snails for 14 or 15 years now—it’s a hobby of mine , ” hans told me . “i produce them for my own consumption , and am also trying to select faster - growing , bigger , superior eating snails . it’s actually a pretty ancient preoccupation . scattered throughout europe and north africa you can find pockets of larger , more colourful helix aspersa , often called helix aspersa maxima . i think that these represent the results of snail breeding carried out in the roman empire . the evidence suggests that the romans bred them for colour , fecundity and growth rate . ”
“some sorts of fungus do a great job on fallen wood . they destroy everything except the cell walls , and you can push your foot right through the log . in there you always find charopa . rotting nikau fronds are not a bad place to find snails either . the bases are tough and smooth , so they provide a good surface to see the regularity of the snail shell on . there are quite a lot of things that resemble shells at first glance—seeds , rolled up arthropods and especially coiled millipedes . some trees such as kauri and tanekaha never have many snails associated with them . roots overgrow their tough leaves before they ever compost . ”
so , having found a likely spot and done a bit of grovelling in the humus , what next ? “finding some snails indicates more in hiding , so i collect a few litres of leaf mould to sort through at home . after drying it out in the boiler house used for heating the glasshouses , i put it through two sieves . the coarse one was put together from plastic mesh used to stop leaves blocking downpipes , and the second one is a fine garden sieve . other people use different methods . david roscoe [ a snail enthusiast from nelson ] somehow manages to float the small snails off in a dish of water . it’s amazing watching him pluck those tiny little shells off the surface of the water with his fingers . ”
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these giants were once widespread in northland before human settlement . many of them are now endangered or threatened , and inhabit a more restricted area of northland and the islands offshore .
mating appears to be triggered by climatic conditions , such as rainfall , and can last for 10 hours or more .
in their natural range . the emphasis is to direct management towards the most genetically and morphologically distinct and viable populations . '
to encourage and support public and community protection of northern giant land snails and their habitat throughout the term of this plan .
doc welcomes any comments or suggestions you may have about the conservation of giant snails . these can be directed to the recovery group via any doc office .
fence off areas of bush where the snails are present . this will stop stock from trampling and crushing them .
these nocturnal snails hide in the leaf litter during the day and come out at night to feed on fallen leaves ( 4 ) .
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colonies a group of organisms living together . individuals in the group are not physiologically connected and may not be related , such as a colony of birds . endemic a species or taxonomic group that is only found in one particular country or geographic area . nocturnal active at night .
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albinism heritable ( passed on from one generation to the next ) , genetic condition in which the pigment melanin is not produced in the skin or hair resulting in white , or partially white individuals . colonies a group of organisms living together . individuals in the group are not physiologically connected and may not be related , such as a colony of birds . endemic a species or taxonomic group that is only found in one particular country or geographic area . nocturnal active at night . translocated when individual living organisms from one area have been transferred and released or planted in another area .


the allodapini is a tribe of bees in the subfamily xylocopinae , family apidae .

they occur throughout sub-saharan africa , south east asia , and australasia .

there is also a rare genus , exoneuridia , that occurs in isolated regions of turkey , iraq , lebanon and iran .

many of the species in the tribe form small social colonies where a group of females cooperatively care for the developing larvae .

the larvae are fed on pollen which , like most other bees , is carried on specialised hairs of the hind pair of legs , but the pollen is fed to the larvae in a progressive fashion and usually placed directly onto their bodies where they then consume it .

the larvae of allodapine bees are remarkable in their complex morphology , and in most species they possess appendages , tubercles and long setae .

the strange morphology of allodapine larvae is probably a result of living in open tunnels where they are in constant contact with other larvae and with adults .

the appendages , tubercles and setae serve to hold and manipulate food , and may also help larvae move around the nest .

these abilities are important because larvae compete with each other to gain food , a situation which is different from all other bees , where individual larvae are isolated in cells and do not have to compete with each other .

there are over 300 described species of allodapine bees , but many more species are undescribed .

they are unique among bees in progressively rearing their larvae in undivided tunnels , so that individual larvae are not physically isolated from each other and are in constant contact with adult females , who provide them with food , groom them , and remove their faeces .

allodapine bees vary greatly in their forms of sociality , from subsocial to highly eusocial .

there are no known species that are purely solitary .

they have been used widely to study social evolution , sex allocation , social parasitism , and historical biogeography .

allodapini

key words : allodapini , brevineura , exoneura , social evolution , phylogenetic conservatism .
stephen g . reyes , steven j . b . cooper , michael p . schwarz ; species phylogeny of the bee genus exoneurella michener ( hymenoptera : apidae : allodapini ) : evidence from molecular and morphological data sets , annals of the entomological society of america , volume 92 , issue 1 , 1 january 1999 , pages 20–29 , urltoken
the largest number of origins of social parasitism has occurred within allodapini ( apidae : xylocopinae ) . there are from eight to ten independent origins of social parasitism in this group . the most problematic group is family halictidae . some cleptoparasitic species have been found inside the nests of eusocial species , but their biology is not clear . three independent origins of social behaviour are possible within this family ( michener 2007 ) .
. . . there are at least eleven independent origins of social parasitism within allodapini , most of which are host specific and range in the degree of morphological adaptations commonly associated with parasitic taxa ( michener , 1970b michener , , 1975amichener , , 2000 ) . müller ( 1872 ) was the first to propose that bee parasites speciate directly from their host and that this explained their frequent similarities ( e . g . . . .
. . . the genus compsomelissa alfken 1924 ( allodapini : allodapina ) is one of the smaller groups of allodapine bees , with only six described species occurring primarily in africa ( michener 1975 michener , 2007 : we use compsomelissa in the restricted and traditional sense , excluding the numerous species placed in halterapis michener 1969 ) . species are distinctive for their largely pale coloration , with large areas of yellow or white , and sometimes reddish metasoma . . . .
. . . the bee tribe allodapini , although distributed widely in the old world , is most diverse throughout africa ( michener , 1975 michener , , 2007 ) . the asian fauna , excluding the near east and arabia , is solely comprised of species in the genus braunsapis michener , and the latter regions add to this a few species of the genera exoneuridia cockerell and compsomelissa alfken ( michener , 2007 ; engel & dathe , 2011 ; engel et al . , in press ) . . . .
. . . the tribes ceratinini and xylocopini contain both solitary and social species , but sociality in these groups never entails lifelong castes . instead , it involves reproductive hierarchies among totipotent females , where the reproductive status of nestmates can change over time and where sterile worker castes are not evident131415 16 17181920 . lastly , all species in the tribe allodapini exhibit at least weak forms of sociality [ 21 ] , but many species have well - defined behavioural castes [ 22 ] and in two species , exoneurella tridentata and hasinamelissa minuta , queen and worker castes are discrete and life - long [ 23 , 24 ] . . . .
the ancestral state for apidae as a whole is not clearly resolved . however , certain groups show clear connections with the new world . the “cleptoparasitic clade” of apidae [ 32 ] is unambiguously reconstructed as south american . the corbiculate clade , as well as the monophyletic group including corbiculates and centridini , are reconstructed as ancestrally new world . xylocopinae , a widespread group , is entirely ambiguous . this could be due to the fact that three of the four xylocopine subfamilies ( ceratinini , allodapini , and xylocopini ) are stem - or wood - nesters and dispersal over water appears to be fairly common in such bees [ 3 , 41 , 44 , 45 ] . large bees , such as xylocopini , may also be capable of long - distance dispersal via flight . our results for anthophorini are unclear because of limited taxon sampling and because this group is geographically widespread . for a more detailed treatment of anthophorine historical biogeography , see dubitzky [ 46 ] .
understanding how sterile worker castes in social insects first evolved is one of the supreme puzzles in social evolution . here , we show that in the bee tribe allodapini , the earliest societies did not entail a foraging worker caste , but instead comprised females sharing a nest with supersedure of dominance . subordinates delayed foraging until they became reproductively active , whereupon they provided food for their own brood as well as for those of previously dominant females . the earliest allodapine societies are , therefore , not consistent with an ‘evo - devo’ paradigm , where decoupling of foraging and reproductive tasks is proposed as a key early step in social evolution . important features of these ancestral societies were insurance benefits for dominants , headstart benefits for subordinates and direct reproduction for both . the two lineages where morphologically distinct foraging worker castes evolved both occur in ecosystems with severe constraints on independent nesting and where brood rearing periods are very seasonally restricted . these conditions would have strongly curtailed dispersal options and increased the likelihood that dominance supersedure occurred after brood rearing opportunities were largely degraded . the origins of foraging castes , therefore , represented a shift towards assured fitness gains by subordinates , mediated by the dual constraints of social hierarchies and environmental harshness .
understanding how sterile worker castes in social insects first evolved is one of the supreme puzzles in social evolution . here , we show that in the bee tribe allodapini , the earliest societies did not entail a foraging worker caste , but instead comprised females sharing a nest with supersedure of dominance . subordinates delayed foraging until they became reproductively active , whereupon they provided food for their own brood as well as for those of previously dominant females . the earliest allodapine societies are , therefore , not consistent with an ' evo - devo ' paradigm , where decoupling of foraging and reproductive tasks is proposed as a key early step in social evolution . important features of these ancestral societies were insurance benefits for dominants , headstart benefits for subordinates and direct reproduction for both . the two lineages where morphologically distinct foraging worker castes evolved both occur in ecosystems with severe constraints on independent nesting and where brood rearing periods are very seasonally restricted . these conditions would have strongly curtailed dispersal options and increased the likelihood that dominance supersedure occurred after brood rearing opportunities were largely degraded . the origins of foraging castes , therefore , represented a shift towards assured fitness gains by subordinates , mediated by the dual constraints of social hierarchies and environmental harshness .
the social biology of many species of allodapine bees from diverse genera has been well studied . however , to infer major evolutionary trends within this tribe as well as plesiomorphic traits in deeper phylogenetic nodes , gaps in our knowledge of social strategies within the poorly understood genus halterapis must first be investigated . the malagasy members of this genus comprise 17 described species , but nesting and social biology of only one of these species has been described . here , we present accounts of the social biology of two other species within this clade , namely , halterapis isaloensis brooks and pauly and halterapis seyrigi ( benoist ) . colony sizes ranged from single - female nests to a seven female nest in h . seyrigi and a nine female nest in h . isaloensis . nests of both species most commonly contained one to three females and approximately one - half of all colonies collected were multifemale . both species display strong size - based reproductive skew within multifemale nests and seem to have strongly female - based sex allocation . when added to previous studies , our findings show that sociality is well developed in all major clades of the allodapines , adding support to the notion that sociality is an ancestral trait of the allodapines . this indicates that extant members of the allodapini do not represent early stages of social evolution and that forms of sociality have frequently reached very complex levels within the tribe .
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origins of social parasitism : the importance of divergence ages in phylogenetic studies . - pubmed - ncbi
warning : the ncbi web site requires javascript to function . more . . .
smith ja 1 , tierney sm , park yc , fuller s , schwarz mp .
flinders university , school of biological sciences , adelaide , sa , australia . jaclyn . smith @ urltoken
phylogenetic studies on insect social parasites have found very close host - parasite relationships , and these have often been interpreted as providing evidence for sympatric speciation . however , such phylogenetic inferences are problematic because events occurring after the origin of parasitism , such as extinction , host switching and subsequent speciation , or an incomplete sampling of taxa , could all confound the interpretation of phylogenetic relationships . using a tribe of bees where social parasitism has repeatedly evolved over a wide time - scale , we show the problems associated with phylogenetic inference of sympatric speciation . host - parasite relationships of more ancient species appear to support sympatric speciation , whereas in a case where parasitism has evolved very recently , sympatric speciation can be ruled out . however , in this latter case , a single extinction event would have lead to relationships that support sympatric speciation , indicating the importance of considering divergence ages when analysing the modes of social parasite evolution .
the evolution of eusociality in allodapine bees : workers began by waiting . - pubmed - ncbi
schwarz mp 1 , tierney sm , rehan sm , chenoweth lb , cooper sj .
school of biological sciences , flinders university , adelaide , sa 5001 , australia . haavarka @ urltoken
pmid : 20943679 pmcid : pmc3061166 doi : 10 . 1098 / rsbl . 2010 . 0757
chronogram of allodapine species with pie charts indicating probabilities for alternative subordinate strategies at key nodes . grey branches denote non - allodapine species that were not used for inferring ancestral social states . coloured squares indicate strategies adopted by subordinate females , and two or more squares indicate polyphenism of strategies . the red circle indicates the most recent common ancestor of the two species with true worker castes , e . tridentata and h . minuta . newly emerged female strategy : green squares , reproduce ; brown squares , forage , blue squares , wait .
jennifer hammock split the classifications by bolds resource for species - level taxa from braunsapis minutula ( friese , 1914 ) to their own page .
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chenoweth , luke b . , simon m . tierney , jaclyn a . smith , steven j . b . cooper , and michael p . schwarz
schwarz , michael p . , susan fuller , simon m . tierney , and steven j . b . cooper
smith , jaclyn a . , simon m . tierney , yung chul park , susan fuller , and michael p . schwarz
disclaimer : itis taxonomy is based on the latest scientific consensus available , and is provided as a general reference source for interested parties . however , it is not a legal authority for statutory or regulatory purposes . while every effort has been made to provide the most reliable and up - to - date information available , ultimate legal requirements with respect to species are contained in provisions of treaties to which the united states is a party , wildlife statutes , regulations , and any applicable notices that have been published in the federal register . for further information on u . s . legal requirements with respect to protected taxa , please contact the u . s . fish and wildlife service .
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current address : department of entomology , university of the philippines at los baños college , laguna 4031 , philippines .
evolutionary biology unit , south australian museum , north terrace , adelaide , south australia 5000 .
an hypothesis of genealogical relationships among taxa provides an historical map along which character evolution ( e . g . , social traits ) can be traced to reveal patterns of common origin or repeated but independent evolution . to investigate the evolution of social traits in the allodapine bee genus exoneurella , we have derived a species phylogeny based on 32 morphological features of adult and immature stages and sequences from 2 mitochondrial dna genes , cytochrome oxidase i ( coi ) and cytochrome b ( cyt b ) . the morphological and coi data support the close relationship of brevineura and exoneurella in accord with previous hypotheses of phylogenetic relationships among allodapine bees . in contrast , the cyt b data supported the sister - group relationship of braunsapis and exoneurella . this was most likely caused by long branch attraction or convergent patterns in the cyt b data set . the morphological and coi data support the basal position of e . tridentata in the exoneurella clade . applying different weights to transversions versus transitions in the analyses of coi sequence data produced 2 trees with 1 totally congruent with the morphological data set . the other tree differed in terms of the arrangement of the 3 distal species of exoneurella : e . lawsoni , e . eremophila , and e . setosa . combined analysis of the 3 data sets yields the following species relationship in exoneurella : ( tridentata + [ lawsoni + ( setosa + eremophila ) ] ) . the a - t rich mitochondrial genome of bees affects the rate of nucleotide substitution leading to the predominance of transversions over transitions and effectively lowering the saturation threshold for transitions . this resulted in transversions accounting for almost all of the informative changes on the tree , even at the species level .
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figure 1 . distribution map for rare ceratina species and exoneuridia hakkariensis in turkey ( from google earth ) .
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an hypothesis of genealogical relationships among taxa provides an historical map along which character evolution ( e . g . , social traits ) can be traced to reveal patterns of common origin or repeated but independent evolution . to investigate the evolution of social traits in the allodapine bee genus exoneurella , we have derived a species phylogeny based on 32 morphological features of adult and immature stages and sequences from 2 mitochondrial dna genes , cytochrome oxidase i ( coi ) and cytochrome b ( cyt b ) . the morphological and coi data support the close relationship of brevineura and exoneurella in accord with previous hypotheses of phylogenetic relationships among allodapine bees . in contrast , the cyt b data supported the sister - group relationship of braunsapis and exoneurella . this was most likely caused by long branch attraction or convergent patterns in the cyt b data set . the morphological and coi data support the basal position of e . tridentata in the exoneurella clade . applying different weights to transversions versus transitions in the analyses of coi sequence data produced 2 trees with 1 totally congruent with the morphological data set . the other tree differed in terms of the arrangement of the 3 distal species of exoneurella : e . lawsoni , e . eremophila , and e . setosa . combined analysis of the 3 data sets yields the following species relationship in exoneurella : ( tridentata + [ lawsoni + ( setosa + eremophila ) ] ) . the a - t rich mitochondrial genome of bees affects the rate of nucleotide substitution leading to the predominance of transversions over transitions and effectively lowering the saturation threshold for transitions . this results in transversions accounting for almost all of the informative changes on the tree , even at the species level .
an hypothesis of genealogical relationships among taxa provides an historical map along which character evolution ( e . g . , social traits ) can be traced to reveal patterns of common origin or repeated but independent evolution . to investigate the evolution of social traits in the allodapine bee genus exoneurella , we have derived a species phylogeny based on 32 morphological features of adult and immature stages and sequences from 2 mitochondrial dna genes , cytochrome oxidase i ( coi ) and cytochrome b ( cyt b ) . the morphological and coi data support the close relationship of brevineura and exoneurella in accord with previous hypotheses of phylogenetic relationships among allodapine bees . in contrast , the cyt b data supported the sister - group relationship of braunsapis and exoneurella . this was most likely caused by long branch attraction or convergent patterns in the cyt b data set . the morphological and coi data support the basal position of e . tridentata in the exoneurella clade . applying different weights to transversions versus transitions in the analyses of coi sequence data produced 2 trees with 1 totally congruent with the morphological data set . the other tree differed in terms of the arrangement of the 3 distal species of exoneurella : e . lawsoni , e . eremophila , and e . setosa . combined analysis of the 3 data sets yields the following species relationship in exoneurella : ( tridentata + [ lawsoni + ( setosa + eremophila ) ] ) . the a - t rich mitochondrial genome
of bees affects the rate of nucleotide substitution leading to the predominance of transversions over transitions and effectively lowering the saturation threshold for transitions . this results in transversions accounting for almost all of the informative changes on the tree , even at the species level .
it has been assumed that allodapine bees represent early stages in the evolution of social behaviour . early studies suggested that sociality evolved from solitary forms , and that the solitary to social transition coincided with a transition from mass to progressive provisioning of brood . recent studies challenge both of these assumptions , they suggest that : ( i ) macrogalea replaces halterapis + compsomelissa as the sister group to all other genera ; ( ii ) sociality is plesiomorphic for the tribe ; and based on extended halterapis research , ( iii ) there are no strictly solitary allodapine species and , therefore , no reversals to solitary living . penalised likelihood dating of bayesian inferred phylograms show allodapine lineages have an origin older than 40 mya . the early origin of sociality in this tribe may explain the diverse array of social organization ( and social parasitism ) found in species across a range of clades , and the age of the group raises curious biogeographic scenarios .
eusocial insects comprise a major faunal element in most terrestrial ecosystems , yet their evolutionary origins are very few [ 1 ] . this means that an ecologically very successful strategy is , paradoxically , unlikely to evolve . two broad approaches have been used to explore how eusociality has arisen . one approach emphasizes ecological factors and kin selection as key evolutionary drivers ( e . g . [ 2 ] ) , whereas a more recent , ‘evo - devo’ , approach emphasizes developmental genetics and how queen and forager castes may be understood in terms of the decoupling of gene suites controlling elements in the developmental groundplans of solitary antecedents [ 3 ] .
these two approaches , one stressing ecological factors and the other developmental genetics , have the potential to bring very different insights to the origins of eusociality [ 3 ] . however , both approaches posit historical scenarios , and assessing these require that we have some knowledge of the evolutionary events leading up to eusociality . a critical issue is whether a key feature of early societies involved rearrangements of elements in the developmental groundplans of solitary ancestors .
bayesian methods ( e . g . [ 4 ] ) can be used to infer the nature of early insect societies , but with the caveat that there is sufficiently informative social variation among extant taxa to have confidence that signals of likely ancestral states can be captured . allodapines meet this requirement , and sociality in species in this group ranges from largely subsocial to highly eusocial [ 5 ] . social nesting , where two or more females help rear brood in a nest , is ancestral for allodapines and has never been entirely lost , probably because of the vulnerability of brood to orphaning and enemies - at - the - nest [ 6 ] . because allodapine larvae are not enclosed within protective cells and are progressively provisioned , they require adults to be present throughout their development .
in all allodapines , females emerge as adults in the company of other , older females . once females reach adulthood they can either disperse or remain in their nest , whereupon there are three broad options available , depending on species [ 7 ] : ( i ) in macrogalea and in some species of exoneurella , females can commence reproduction without any apparent social constraints ; ( ii ) in most other species , females join a reproductive hierarchy where they delay foraging roles until they also lay eggs ; and ( iii ) in some species , including the two highly eusocial species , females can assume a foraging role without becoming reproductive . we call these three strategies reproduce , wait and forage , respectively . although waiting involves eventual direct reproduction , it may also entail alloparental care , both immediate and delayed . while waiting , females could help in nest maintenance or other intra - nidal tasks ( e . g . [ 8 ] ) , and after assuming dominance , food they bring back to the nest could be used by their own brood as well as any remaining brood from previously dominant females . allodapine broods are reared in a communal tunnel where they are in physical contact and able to move , so that food brought into the nest is available to all larvae that are present [ 9 ] .
here , we ask whether newly emerging females in early allodapine lineages were likely to adopt reproduce , wait or forage roles . each of these strategies could have very different implications for understanding the origins and subsequent elaboration of sociality .
we used detailed published studies ( see electronic supplementary material ) to identify strategies adopted by newly emerged females in 16 species covering all major allodapine clades . social organization tends to be phylogenetically conserved within allodapine genera [ 10 ] and less detailed studies ( e . g . [ 11 ] ) do not suggest forms of sociality that differ in structure from our included species . in some allodapines , newly emerging females can adopt two or more of the wait , reproduce and forage strategies ; e . g . in exoneurella setosa they can adopt any one of the three strategies [ 12 ] . only two allodapines , exoneurella tridentata and hasinamelissa minuta , show the hallmarks of highly eusocial behaviour : queen - worker dimorphism with sterility or near - sterility of workers [ 5 ] .
we developed phylogenies of these 16 species , but when doing so we included additional species ( see electronic supplementary material ) , for which detailed social data were not available , to avoid long - branch attraction for thinly sampled clades . we used halictine bees as the outgroup and included corbiculate and ceratinine species to provide fossil calibration points . these taxa were all deleted from trees before inferring ancestral allodapine social traits . we used the same gene fragments ( coi , cytb and the f2 copy of ef - 1 α ) and bayesian protocols as chenoweth et al . [ 6 ] , outlined in the electronic supplementary material . after phylogenetic analyses , allodapines lacking social data were pruned from trees , and the resulting phylograms were transformed into chronograms using the same calibration points and method for estimating divergence dates as chenoweth et al . [ 6 ] , also outlined in the electronic supplementary material .
, for exploring ancestral character states . various priors were explored , with the criterion that acceptance rates are bounded by 20 and 40 per cent [
] . a rate deviation prior of 15 with an exponential ( 0 , 10 ) reverse jump hyperprior met this requirement , but trials using gamma priors with similar acceptance rates produced almost identical results . we used 40 × 10
, sampling every 1000th generation . likelihoods of alternative ancestral states were assessed using bayes factor ( bf ) tests , ‘fossilizing’ each strategy for each relevant node in turn [
iterations , choosing post - burn - in periods on the basis of harmonic mean plots . all fossilized runs were replicated at least twice to check for the consistency of results , but no discrepancies were found .
our results are summarized in figure 1 , where the relative likelihoods of alternative ancestral strategies ( reproduce , wait and forage ) are summarized using pie charts . charts are given for ancestral nodes leading to the two highly eusocial species , e . tridentata and h . minuta , but only where bf tests ( electronic supplementary material , table s2 ) supported one strategy over both alternatives . our analyses indicate that each of these species was preceded by greater than or equal to four antecedent nodes with support for waiting . these included the root allodapine node and the most recent common ancestor ( mrca ) for these eusocial species . one complication is the possibility of polyphenism of strategies at internal nodes , as happens in some extant species . we explored the likelihood of ancestral polyphenism by coding extant species as monophenic or polyphenic and then used the same ‘fossil’ protocol as above to infer ancestral states . we found that monophenism was more probable in both the root node and the mrca for the two highly eusocial species ( bf = 3 . 294 and 2 . 556 , respectively ) .
it has been hypothesized that origins of worker castes may be explained by the decoupling of separate elements in developmental groundplans of solitary ancestors ( e . g . [ 14 , 15 ] ) , such as gene networks for oviposition and foraging . in this way , castes could arise from differential expression of behaviours that were , to a large extent , present before the origin of sociality . if such decoupling of elements is the key to the origins of sociality , as suggested by the evo - devo paradigm , we would expect to see signs of this in the earliest allodapine lineages . we found no evidence for this . instead , those early societies were more likely to comprise female assemblages where foraging and reproduction were not decoupled , and where the joint activation of oviposition and foraging , characteristic of solitary - nesting females , waited on dominance supersedure . this does not mean that the eventual appearance of highly eusocial behaviour did not entail the developmental shifts envisaged by evo - devo , but it does mean that substantial evolutionary time occurred between the origin of sociality and the later origins of foraging castes .
our analyses indicate that waiting by subordinates was the ancestral trait and persisted in most lineages for greater than 40 ma . waiting , therefore , exhibits substantial evolutionary stability . we suggest this is owing to three features : ( i ) subordinates do not take on a foraging role until they are reproductive , so that associated risks are delayed until foraging also reaps direct fitness benefits ; ( ii ) any brood from previously dominant females that are still present after supersedure will benefit from alloparental care by newly dominant females , providing indirect ‘headstart’ benefits [ 16 ] ; and ( iii ) dominant females may gain ‘insurance benefits’ [ 17 ] by tolerating the presence of waiting females , who could complete the rearing of orphaned brood when the dominant dies .
interestingly , both highly eusocial species , e . tridentata and h . minuta , occur in arid ecosystems where nesting sites are scarce and where rainfall is highly seasonal and very limited [ 18 , 19 ] . scarcity of nesting sites would lower the rates of successful dispersal , and seasonally restricted rainfall means that , by the time waiting subordinates attain dominance , there may be few floral resources to begin a new round of brood rearing . given these constraints , assumption of a forage - now role might become the best strategy for gaining indirect fitness via ‘assured fitness returns’ [ 20 ] .
assuming a foraging role while waiting in a reproductive queue may have important consequences for future strategies . foraging entails physiological and mortality costs , and these are likely to reduce the likelihood of attaining future dominance , leading to a trade - off between future direct fitness and more - immediate assured indirect fitness . for example , allocation of physiological resources to foraging would leave fewer reserves for later ovarian development , and predation risks during foraging would lower the likelihood of surviving until dominance supersedure becomes possible . such trade - offs could canalize the worker strategy : as a subordinate strategy becomes increasingly honed for foraging and its assured fitness returns , the possibilities for assuming reproductive dominance would lessen . this scenario is not inconsistent with evo - devo , but it does suggest an important role for ecological selective factors in the eventual origins of foragers .
, and trevor lehmeyer for figure production . this research was supported by the australian research council .
social biology of exoneurella tridentata , an allodapine bee with morphological castes and perennial colonies .
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we present the first data on the social biology of the allodapine bee , brevineura froggatti . colony sizes are small , and only 12 . 5 % of nests contained more than two females . brood rearing occurs throughout the year , including winter , as it does in the other species of brevineura studied to date . in both brevineura species , per capita brood production is much higher in multi - female nests than single female nests , raising the question of why more colonies aren ' t multifemale . the occurrence of small colony sizes , despite large benefits to group living , differs strongly from species of the sister clade exoneura . these findings , combined with previous allodapine studies , indicate conservatism in voltinism , brood phenology and colony size within , but not between , australian allodapine genera .
received 22 july 1999 ; revised 4 november 1999 ; accepted 16 november 1999 .
school of biological sciences , flinders university of south australia , gpo box 2100 , adelaide , s . a . 5001 , e - mail : michael . schwarz @ urltoken
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social parasitism is the best - studied cleptoparasitic strategy . it stands on the border of social behaviour , usurpation and brood parasitism . social parasitism always includes a combination of these three behavioural patterns . usurpation , as a component of social parasitism , is described above . the brood parasitism component is quite different from cuckoo behaviour , as social hosts are progressive provisioners and feed their brood directly from the crop ( michener 1974 ) . in mass provisioning species ( halictidae ) the biology of social parasites is unknown .
social parasites have evolved independently from eusocial ancestors ( except some sphecodes ) roughly sixteen times in two families ( michener 2007 ) . the well - known group of socially parasitic bees of the family apidae includes cuckoo bumblebees ( bombus sg . psithyrus ) . there are two other bombus species with possible obligate or occasional socially parasitic behaviour .
social parasitism at the intraspecific level has been documented in bombus terrestris ( linnaeus ) . male - producing reproductive workers enter unrelated conspecific colonies in which they then produce adult male offspring . these socially parasitic workers are significantly more reproductive and aggressive than resident workers that reproduce within their own colonies ( lopez - vaamonde et al . 2004 ) .
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among the numerous nonparasitic allodapine bees there are 11 known species with parasitic or probably parasitic habits . these species live in nests of their close relatives , the female parasite replacing an egg - layer of the host . seven of the parasitic species are distributed among four otherwise nonparasitic genera , while four species of parasites are placed in three exclusively parasitic genera . the parasites have mostly arisen independently from different nonparasitic forms . there is much convergence among the parasitic forms involving such characters as the flattened or concave face , reduced eyes , reduced mouthparts , reduced wing venation , and reduced pollen - carrying scopa . in the most specialized parasitic genera the mouthparts are so small as to be almost surely useless for obtaining food from flowers . such bees must feed in the host nest , and are not found on flowers . their wings must be adequate to take them to a new host nest but the reduced venation and eyes must reflect the reduced locomotary and sensory needs of a bee that does not visit flowers . in this paper a new , presumably parasitic allodapula is described as is a parasitic braunsapis , a parasitic allodape , and a eucondylops . a previously described macrogalea is recognized as a parasite for the first time . a new genus and species of parasites nasutapsis straussorum , allied to braunsapis , is also described . all these forms are from africa .
. . . morphological terminology generally follows that of hurd and moure ( 1963 ) and michener ( 2007 ) . the use of ventroapical plate of the male gonocoxite and lateral carina of the penis valve follows michener ( 1975 ) and minckley ( 1998 ) ; supraorbital line refers to the upper ocular tangent and is used here to indicate the position of the laterall ocelli in frontal view . external morphological features were studied using a nikon smz 745t stereomicroscope . . . .
. . . mesofemoral brush , scopa ) , and enhanced features related to aggression and defence ( e . g . enlarged mandible , strengthened integument ) ( michener , 1970 michener , , 1978 ) . convergence of adaptive morphologies associated with parasitism can wreak havoc with morphology - based phylogenetic analyses ( alsina and michener , 1993 ) . . . .
. . . the first detailed studies of allodapines were carried out by charles michener who examined a large number of species from both africa and australia and published a wide variety of monographs and papers covering nesting and social biology ( e . g . michener , 1965 michener , , 1971 ) , social parasitism ( michener , 1970b ) , nesting substrates ( michener , 1970a ) , adult and immature morphology ( eg . michener , 1975a michener , , b , c , d , 1976 ) , and egg - size variation ( michener , 1973 ) . . . .
. . . the majority of molecular phylogenetic studies on the relationships of insect social parasites to their hosts have been based on ants , with fewer studies on wasps , and corbiculate and halictine bees . however , there have been almost no studies on parasitic allodapine bees , even though they show at least eleven independent origins of social parasitism ( michener , 1970 ; smith and schwarz , 2006a ) . this number of origins could be due to the nature of allodapines , where brood are not enclosed within cells and multi - female nesting is ubiquitous ( schwarz et al . , 1998 ) . . . .
. . . the lack of research on allodapine bee parasites is therefore surprising , especially considering that 7 . 9 % of the currently described species have been determined to be social parasites , which compares to only 1 . 7 % for all known ant species ( brandt et al . , 2005 ) . the socially parasitic allodapines exhibit a diverse range of morphological adaptations , with some species only distinguishable from their hosts by minor differences , such as slightly reduced scopae , while other species are extremely modified , with characteristics such as greatly reduced mouthparts , unique head and tergite projections , and a complete lack of functioning scopae ( michener , 1970 ) . this range in the degree of adaptation to social parasitism is reflected in taxonomic structure , with some parasites accorded generic status , and others being placed in the same genus as their hosts . . . .
. . . , 1993 ) and ants ( buschinger , 1986 ; ho èlldobler & wilson , 1990 ; bourke & franks , 1991 ) , termed inquilinism . in bees , social parasites are known from the genus psithyrus ( apidae : bombini ) , as well as the allodapine bees ( michener , 1970 , 1974 ) . in psithyrus , females enter the nests of their hosts and co - exist with the host queen , or , in some cases , kill her ( fisher , 1987 , 1988 ; franks , 1987 ; fisher & sampson , 1992 ; ku èpper & schwammberger , 1995 ) . . . .
lasioglossum versatum , a bee whose colonies occur in small , dense aggregations , shows tolerance and some interactions among individuals of different colonies and thus social activity at a level above that usual among social insects . guards admit individuals from any colony . burrows made by different colonies sometimes interconnect . most or all workers are attached primarily to one colony but . . . [ show full abstract ]
caupolicana floridana new species is a large bee from the southern part of the florida peninsula , known from only two areas , dade county where it may be extinct and highland county . it is a close relative of c . electa ( cresson ) which occurs in the southeastern states including northernmost florida . data on seasonal and floral behavior are included .
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bees are the primary pollinators of angiosperms throughout the world . there are more than 16 , 000 described species , with broad variation in life history traits such as nesting habitat , diet , and social behavior . despite their importance as pollinators , the evolution of bee biodiversity is understudied : relationships among the seven families of bees remain controversial , and no empirical global - level reconstruction of historical biogeography has been attempted . morphological studies have generally suggested that the phylogeny of bees is rooted near the family colletidae , whereas many molecular studies have suggested a root node near ( or within ) melittidae . previous molecular studies have focused on a relatively small sample of taxa ( ~ 150 species ) and genes ( seven at most ) . public databases contain an enormous amount of dna sequence data that has not been comprehensively analysed in the context of bee evolution .
we downloaded , aligned , concatenated , and analysed all available protein - coding nuclear gene dna sequence data in genbank as of october , 2011 . our matrix consists of 20 genes , with over 17 , 000 aligned nucleotide sites , for over 1 , 300 bee and apoid wasp species , representing over two - thirds of bee genera . whereas the matrix is large in terms of number of genes and taxa , there is a significant amount of missing data : only ~ 15 % of the matrix is populated with data . the placement of the root as well as relationships between andrenidae and other bee families remain ambiguous , as several alternative maximum - likelihood estimates fall within the statistically credible set . however , we recover strong bootstrap support for relationships among many families and for their monophyly . ancestral geographic range reconstruction suggests a likely origin of bees in the southern hemisphere , with melittidae ancestrally located within africa , and halictidae , colletidae , and apidae within the new world .
our study affirms the monophyly of each bee family , sister - taxa relationships between apidae and megachilidae ( the ‘long - tongued bees’ ) , between colletidae and stenotritidae , and between colletidae + stenotritidae and halictidae . our analyses reject a colletidae - basal hypothesis for family - level relationships and instead support melittidae as sister to the remaining bees . southern hemisphere vicariance likely played an important role in early diversification within many bee families .
bees ( hymenoptera : apoidea : anthophila ) provide a rich system for exploring the evolutionary consequences of a wide variety of life history characteristics . bees provision larvae with pollen and nectar , a trait that evolved in the early - to mid - cretaceous from carnivorous , wasp ancestors [ 1 - 5 ] . it has been suggested that this transition from carnivory to pollenivory led to rapid diversification and expansion of bee lineages as a result of the exploitation of pollen as a novel resource ( i . e . , a key innovation [ 6 , 7 ] ) . within bees , a number of life history traits have evolved multiple times both within and among bee families , including diet specialization , eusociality , and social parasitism ( reviewed in [ 8 ] ) . a robust phylogeny is fundamental to determine how changes in these life history traits have affected behavior , geographic range , phenology , susceptibility to habitat loss or pathogens , and gene or genome evolution .
previously published hypotheses for relationships among bee families . a . andrena crataegi ( andrenidae ) [ photo credit : phil huntley - franck ] , b . habropoda tarsata ( apidae ) [ photo credit : jelle devalez ] , c . hylaeoides concinna ( colletidae ) [ photo credit : kristi ellingsen ] , d . halictus sp . ( halictidae ) [ photo credit : nicolas vereecken ] , e . lithurgus chrysurus ( megachilidae ) [ photo credit : nicolas vereecken ] , f . dasypoda hirtipes ( melittidae ) [ photo credit : nicolas vereecken ] , g . ctenocolletes smaragdinus ( stenotritidae ) [ photo credit : laurence packer , york university : bee tribes of the world photographic project ] . h - o . alternative topologies for relationships among bee families , including the placement of the root .
f ] , and stenotritidae ) form the loosely - defined “short - tongued” bees . relationships among short - tongued bees are unclear . monophyly of short - tongued bees has not been supported by most previous morphological or molecular studies , although one analysis of three nuclear genes supported a tree in which short - tongued and long - tongued bees are reciprocally monophyletic ( figure
an obvious strategy to improve our ability to distinguish among alternative hypotheses is to increase both taxonomic sampling and the number of genes sampled for phylogenetic analysis ( [ 19 - 24 ] ) . increased taxon sampling can improve statistical support for accurate phylogenetic estimates even when the taxa added have incomplete information [ 25 - 27 ] . we estimate phylogenetic relationships among an unprecedented number of apoid taxa by combining publically - available data from multiple , independent sources . we confined our analyses to dna sequences of nuclear protein - coding genes , which have more power than mitochondrial genes in recovering older relationships [ 28 - 30 ] and are considerably more straight - forward to align compared to ribosomal genes . we tested alternative phylogenetic relationships from the literature for statistical significance . finally , we provide the first global biogeographic analysis to explore bee historical biogeography at the level of family and subfamily .
we have assembled the largest molecular data set for analyzing higher - level ( family , subfamily , tribal ) relationships among bees to date . our data set includes 349 of the approximately 500 currently recognized bee genera [
) . we obtained strong bootstrap support for several additional clades : the long - tongued bees ( apidae + megachilidae ) , colletidae + stenotritidae , and a clade containing halictidae + colletidae + stenotritidae . melittidae is weakly supported as sister to all other bees , consistent with the hypothesis that the root of bee phylogeny falls near melittidae rather than colletidae ( table
k ) , but with a bootstrap proportion of only 0 . 47 ( table
maximum - likelihood estimate of relationships among bee species . circles at nodes represent bootstrap proportions after 100 nonparametric bootstrap replicates : black > = 0 . 8 , grey > = 0 . 5 . nodes with bootstrap proportions less than 0 . 5 are without circles . tips are unlabelled to reduce visual complexity ; the labelled species tree is available in newick format in additional file 1 .
at the subfamily and tribal levels , our phylogeny is broadly congruent with molecular phylogenies published for particular families , and where it is not , bootstrap support values fall below 0 . 75 . within apidae , discrepancies between this study and that of cardinal et al . [ 32 ] include the placement of anthophorini , caenoprosopidini , ammobatoidini , manuelini , and apini / euglossini . our phylogeny is consistent with their finding that apinae is not monophyletic : we recovered a large clade composed of the majority of cleptoparasitic species of apinae and nomadinae . our inferred relationships among megachilid tribes differs from litman et al . [ 33 ] only in the placement of lithurgini as basal to , rather than sister to , pararhophitini . our phylogeny lacks resolution within colletidae , but all well - supported nodes are also found in the estimate of almeida et al . [ 34 ] . within halictidae , thrincostomini is sister to halictini , in contrast to danforth et al . [ 35 ] , but our phylogeny is otherwise congruent with theirs . finally , the only discrepancy between relationships recovered within melittidae in this study and that of michez et al . [ 17 ] is that we do not recover dasypodaini as monophyletic .
many of the family - level relationships in our tree are reasonably well - supported based on bootstrap proportions . despite this , we could not reject five of our plausible alternatives to rooting the bee tree with high statistical support ( table
) . the placement of colletidae as basal to the remainder of the bees and the monophyly of long - tongued bees + melittidae can confidently be rejected as failing to fit our data , even after bonferroni correction for multiple testing ( p < 0 . 01 ) . the remaining possible topologies all fall within the confidence set of both the approximately unbiased and weighted shimodaira - hasegawa tests . the bic places only one hypothesis within this 95 % , in agreement with the maximum - likelihood estimate ( figure
probabilities that a given topology falls within the 95 % confidence set ( reject after bonferroni correction when p < 0 . 01 ) under the weighted shimodaira - hasegawa test ( wsh ) , approximately unbiased test ( au ) , and bayesian information criterion ( bic ) . letters refer to the topologies in figure
. for each hypothesis , values that indicate the topology falls within the 95 % confidence set are in bold . * = maximum - likelihood estimate .
phylogenetic inference based on dna sequence data can be affected by saturation—when phylogenetic signal among sequences is stochastically lost over time . saturation occurs more rapidly in fast - evolving sites , such as the third codon position , and removal of these sites may increase phylogenetic accuracy [ 19 ] . we estimated phylogenetic relationships after excluding the third codon position from our dna sequence alignment . the resulting maximum - likelihood estimate was unresolved , suggesting that third codon positions do contain phylogenetic signal ( additional file 1 ) .