Apidologie 40 (2009) 347–354 Available online at: c INRA/DIB-AGIB/EDP Sciences, 2009 www.apidologie.org DOI: 10.1051/apido/2009018 Review article

Diversity and conservation status of native Australian *

Michael Batley 1,KatjaHogendoorn2

1 Australian Museum, 6 College St, Sydney, N.S.W., 2010, Australia and Department of Biological Sciences, Division of Environmental and Life Sciences, Macquarie University, North Ryde, N.S.W. 2109, Australia 2 School of Agriculture, Food and Wine, University of Adelaide, SA 5005, Australia

Received 8 August 2008 – Revised 14 October 2008 – Accepted 26 October 2008

Abstract – Australia’s idiosyncratic fauna is characterised by a combination of numerous endemic taxa and by the complete absence of some families. Many species, and in particular several oligolectic species, remain undescribed and more than half the named taxa are in need of revision. The main threats to the native bee fauna include removal of nesting and foraging opportunities through land clearing and agriculture, the spread of exotic plant species and the consequences of climate change. Early steps to conserve the native bee fauna include commercial applications, the raising of public awareness and preservation of natural habitat. However, these actions are severely hampered by a lack of both identification keys and taxonomic expertise. Considerable investment in taxonomic research is needed to improve this state of affairs. native bees / Australia / conservation / / Apoidea

1. DIVERSITY OF BEES 100 bee species are either known or suspected IN AUSTRALIA to be oligolectic (AFD, 2006). Michener (1965) noted a clear difference Australia has a distinctive bee fauna char- between the “typically Australian element” acterized by an unusually high proportion found throughout most of the continent and of species in the family (Tab. I). the depauperate bee fauna of the northern rain- Several groups with widespread distributions forests that shares features with that of New throughout the rest of the World, notably An- Guinea and the Indo-Malaysian region. At drenidae and Mellitidae, are not found in Aus- the species level, there is a less distinct divi- tralia while the family Stenotritidae, and the sion between the fauna of the open eucalypt subfamily Euryglossinae are endemic to the forests and woodland of eastern and south- region (Michener, 1965, 2000). More than eastern coastal regions and that of the arid three-quarters of the known species belong zone which covers most of the remaining area. to the three most highly derived bee fami- There are no sharp lines of demarcation and lies, Stenotritidae, Colletidae and Halictidae species belonging to groups with significant (Danforth et al., 2006) and a small number of diversity in New Guinea have been found in colonisation events have given rise to lineages, rainforest remnants as far south as Sydney. like the genus Exoneura (Schwarz et al., 2006) or parts of the genus Lasioglossum (Danforth While the taxonomy of Australian bees and Ji, 2001), that are endemic to Australia has received some attention in the last 20 and adjacent areas. Despite the incomplete na- years, there is still a large number of unde- ture of flower-visiting records, approximately scribed species. The Australian Faunal Direc- tory (AFD, 2006) lists 1647 names, of which Corresponding author: K. Hogendoorn, about 45% come from revisions published [email protected] after 1965, 18% have been treated in doc- * Manuscript editor: Mark Brown toral theses that remain unpublished, and the

Article published by EDP Sciences 348 M. Batley, K. Hogendoorn

Table I. The number of Australian genera and named species (AFD, 2006) covered by keys. References to the keys are given in Michener (2000).

family # genera # genera with keys # named # species covered % of species covered to at least part species by keys by keys Apidae 13 4 197 49 25% Colletidae 31 20 879 434 49% Halictidae 11 3 385 188 49% Megachilidae 5 1 168 25 15% Stenotritidae 2 1 21 10 48% remaining 37% are greatly in need of revi- affect bee populations, with demonstrable eco- sion. Genera such as Exoneura, Lipotriches, nomic consequences (Kremen et al., 2004). Stenotritus, Paracolletes, Trichocolletes and Similar studies have shown that the presence much of Euhesma have not been studied in re- of native Australian rainforest is important cent times. for the unmanaged pollination of tropical fruit Extrapolation of the results of four recent (Blanche et al., 2006). investigations, including unpublished theses, Conservation of native vegetation in Aus- covering almost 30% of the fauna suggests tralia has received considerable public and that between 300 and 400 species remain un- regulatory attention over the past 20 years, pri- described, but that the total number of valid marily with the objectives of controlling sec- names will remain virtually unchanged when ondary dryland salinity, maintaining biodiver- synonyms are removed. However, not only sity and reducing greenhouse gas emissions. are there large uncertainties in such extrapo- A recent review of progress towards national lations, but there is probably a bias towards objectives for biodiversity conservation (Grif- polylectic species. Oligolectic species are of- fin NRM Pty Ltd., 2004) concluded that, de- ten overlooked until the nature of their special- spite patchy success in many areas, clearing of isation is discovered (Houston, 1989, 1992, native vegetation will be effectively controlled 1993;Exley1998, 2004; reviewed in Murray in most jurisdictions by 2010, provided that et al., 2009). currently proposed and enacted regulations are A measure of the extent of missing informa- properly implemented. Australia is still some tion is given by the number of subgenera for distance from achieving a no net loss target which there are no published keys to species for native vegetation, but the recent policy and (Tab. I). Overall, 57% of all named species are regulatory interventions should ensure that all not covered by keys. future clearing proposals are subject to appro- Knowledge of the taxonomy of Australian priate levels of assessment relative to the con- bees is much more extensive than information servation status of the vegetation community. about their biology. Many species are known from very few specimens and distributions and Some areas have been less affected by clear- flowering-visiting records for regions outside ing than others so that only 13% of the to- Western Australia are limited (Houston, 2000: tal land area has been cleared. The largest AFD, 2006). proportion of Australia, the rangelands of the arid zone, remains relatively free of broad- scale clearing. The eastern and south-eastern 2. THREATS TO BEES coastal areas were predominantly eucalyptus IN AUSTRALIA forests and woodlands. Approximately 80% of the pre-European extent of eucalypt forests 2.1. Deforestation and agriculture and woodlands remain, despite high rates of clearing in Queensland and New South Wales The loss of floral resources and nesting sites that were a cause for concern. Between 1981 associated with deforestation will obviously and 1999 the average rate of clearing was Bees in Australia 349

38000 ha/year in NSW and 343 000 ha/year in nectar-producing flowers, making pesticides Queensland, though some of this was removal of secondary importance. of regrowth. The most severely affected vege- tation groups are the low closed forests, closed shrublands and the heaths, of which only 50% 2.2. Exotic species now remains, but these covered only 1% of the continental area. Australia is the only country yet to be in- However, vegetation removal is not the only vaded by Varroa destructor and has a large form of ecological disturbance and an area population of feral Apis mellifera. The num- may retain the same vegetation type and yet bers of feral honeybees are such that they may have a different species composition. For ex- be affecting the populations of birds, mammals ample, it has been estimated that of the two and other by virtue of the sheer amount million ha of lowland grassland in south- of floral resources that they consume (Paton, eastern Australia at the time of European set- 1996; Stout and Morales, 2009). Paini (2004) tlement, the remaining natural remnants cover has reviewed the 10 studies that addressed var- 10000 ha. (McDougall and Kirkpatrick, 1994). ious aspects of the impact of European honey- Furthermore, in the arid centre of Australia, bees on native bees in Australia and concluded substantial changes in plant composition have that many of the studies suffered from low been attributed to the impacts of water-centred replication or confounding factors. It is likely grazing. The effect of such changes on bee that the most important impact of honeybees populations could be considerable. For exam- on native bees is indirect, through their role in ple in the southern arid regions of Australia, the propagation of serious exotic weeds such the lack of regeneration of Western Myall as Scotch Broom (Cytisus scoparius, Simpson due to rabbit, goat and sheep grazing (Lange et al., 2005), and lantana (Lantana camara, and Purdie, 1976), may seriously affect the Goulson and Derwent, 2004) at the cost of survival of the endemic allodapine bee Ex- native vegetation (Stout and Morales, 2009). oneurella tridentata, because this species de- The imminent arrival of the Varroa mite in pends largely on the dead branches of this Australia, which is expected to largely wipe tree for nesting substrate (Hurst, unpubl. data). out feral honeybees, will provide an interesting This is an important issue, because E. triden- opportunity to investigate the impact of feral tata is the only known eusocial bee species honeybees on the native flora and fauna. outside the Apinae that has allometric castes A second exotic species of concern (Houston, 1977). However, the extent to which (Hingston and McQuillan, 1998; Hingston these changes in the landscape have influenced et al., 2002)isBombus terrestris which has the distribution and biology of bee species will become widespread on the island state of never be known, because both information on Tasmania since its introduction in 1992, the status quo before human intervention and and has been shown to displace native bees on the current situation are seriously deficient. from flowers (Hingston and McQuillan, Floral diversity may also be important for 1999). However, again the main reason for bees (Murray et al., 2009). It has been sug- concern about this incursion lies in the fact gested (Bernhardt, 1987)thatmanyAcacia that this species is likely to increase the seed species require the presence of co-blooming production of some weeds and sleeper weeds nectiferous flowers if bee populations are to be (Goulson, 2003; Stout and Morales, 2009), supported. which will in turn influence the native bee There is also an absence of information fauna. about the impact of agricultural pesticides on As an island continent, Australia has a nat- bee populations. While it is tempting to blame ural advantage for the exclusion of exotic pesticide use for low bee densities, large-area species and has a strong quarantine system agriculture itself may be responsible. Areas in operation. Strict protocols were adopted devoted to the production of cereal crops may to ensure that the importation of Megachile support few bees because of the absence of rotundata for pollination of alfalfa did not 350 M. Batley, K. Hogendoorn bring exotic parasites and diseases (Anderson, 3. PRESERVATION OF NATIVE BEES 2006). Quarantine procedures were, however, IN AUSTRALIA unable to prevent introduction of the Emerald Furrow Bee, Halictus smaragdulus, which has There are two possible strategies for con- been found in the Hunter Valley of New South serving existing bee species – development of Wales (Gollan et al., 2008) and the Carder Bee, commercial applications and the development Afranthidium repetitum (Walker, 2008)which of public interest. Early steps have been taken has become common over a wide area around in both directions. Brisbane. Specimens of both have now been Concern about the potential loss of polli- found in Sydney (MB, unpubl. data). nation services by feral honeybees that would follow the arrival of Varroa mites in Aus- tralia has resulted in a recommendation to the government to fund research into possible 2.3. Climate and climate change ways of dealing with this incursion. The rec- ommendations include investigation of native species that could be used as alternatives to Much of Australia has an unstable environ- Apis for certain crops. Although doubts about ment, with large variations in rainfall. Floods the possibility have been expressed (Gordan are common in the north of the country and can and Davis, 2003), solitary bees are success- wipe out aggregations of ground nesting bees fully used in several crops overseas (Delaplane (e.g. Fellendorf et al., 2004). While climate and Mayer, 2000) and methods for the devel- change is expected to increase the frequency opment of bees as crop pollinators are well of such events and adverse effects are expected established (Bosch and Kemp, 2002). The for ecosystems like rainforests and alpine re- sceptics may have overlooked the possibility gions, it is more difficult to foresee the im- that an important constraint on native popula- pact on other areas (Murray et al., 2009). One tions may be set by the availability of nesting firm prediction is that bushfires, which often sites (Steffan-Derwenter and Schiele, 2008; destroy large areas of native woodland, will Kremen et al., 2004), a limitation that might be become more frequent and of greater severity. overcome without too much difficulty. Recent Bushfire management is a major social issue research shows that both Australian Xylocopa in Australia with competing demands of prop- and Amegilla are useful pollinators for tomato erty protection and environmental conserva- in greenhouses (Bell et al., 2006; Hogendoorn tion. A number of investigations have been un- et al., 2000, 2006, 2007). Stingless bees can dertaken (e.g., Auld, 2001; Auld and Denham, be used as pollinators of several tropical crops 2006) to assess the effect of fire frequency such as macadamia and mango (Heard, 1999). on plants, but the consequences for bees in Preliminary research on the use of six native unknown. It is suspected that the carpenter megachilid species as pollinators for Lucerne bee Xylocopa aeratus has become extinct in pollination (Bray, 1973) demonstrated their ef- Victoria through a combination of land clear- ficiency as pollinators of this crop, but the ing and burning of the areas that are cur- study was not followed up due to a lack of rently still suitable to support a population suitable techniques for propagation and ma- (Leijs, unpubl. data). An increase in tempera- nipulation of the activity patterns, which have ture through global warming will no doubt ex- now been developed overseas (e.g. Bosch and acerbate these problems. Furthermore, in re- Kemp, 2002). sponse to the drought, urban gardeners and The level of public interest in conserva- parks management have taken to extensive tion of Australian native bee species is quite mulching of bare soil. Although this is a com- high and it should be possible to build up sup- mendable strategy to achieve water conserva- port both for general conservation measures tion, it has caused the loss of numerous aggre- and for development of urban areas as refugia gations of ground nesting bees (MB and KH, (Tomassi et al., 2004). Dr Anne Dollin has for unpubl. data). many years promoted their conservation and Bees in Australia 351 exploitation through the Australian Native Bee can only be supplied by expert taxonomists. Research Centre and there is an active Yahoo The recent, sad loss of Professor Elizabeth Ex- interest group whose members regularly ex- ley has deprived us of a major contributor to change pictures and news via the internet. In both the taxonomy of Australian bees and the October 2006, a two day workshop on native training of Australian taxonomists. The coun- bees attracted 50 participants from all over the try now has six living bee taxonomists with an country and occasional talks on the subject of average age of well over fifty, but only two native bees are usually well-attended. At least are employed in positions that would permit one local Council is actively encouraging its even limited time for bee taxonomy. A num- rate-payers to keep Trigona carbonaria hives ber of government-fundedprojects designed to in their gardens. Australian suburban areas are improve public access to available information generally well vegetated and likely to sustain are in the pipeline, which will only increase the greater bee diversity than more densely popu- need for fundamental taxonomic data. Unless lated cities (Matteson et al., 2008). there is a concerted effort to provide training Bees will, of course, benefit from conser- and employment in the appropriate skill areas, vation measures of a more general nature, like the information of the conservation status of the reduction of vegetation clearance or the es- Australian native bees will not become avail- tablishment of the 2800 km wildlife corridor able, and moreover the present capacity will along almost the entire east coast of Australia, be lost. allowing plants and to move as cli- mate changes. 4. CONCLUSIONS The major constraint on bee conservation, however, is the severe shortage of information Australia has an extensive and interesting and expertise. The authors of the Australian bee fauna, which is currently threatened by Terrestrial Biodiversity Assessment (Sattler large scale agriculture and possibly by changes and Creighton, 2002) found that “data on in- in climate. Of major concern is the absence vertebrates are patchy: conclusions cannot be of basic information about the biology of the drawn at the Australia-wide scale”. bee fauna. Although the majority of species The need for expertise is just as urgent. Ex- are polylectic, it is the significant minority of amination of the list of 76 designated wildlife oligolectic species that are most under threat refugia in arid and semi-arid areas (Morton (Zayed et al., 2005; Zayed, 2009)andmost et al., 1995) reveals that no were likelytohavedifficulty adapting to new hosts included among the invertebrates to be pro- (Praz et al., 2008). Many oligolectic species tected in these areas, though many species of may remain undiscovered. More importantly, gastropods and pseudo-scorpions were men- information about distribution and breeding tioned. It must be concluded that advocacy by behaviour of the majority of species is incom- taxonomists and ecologists with an interest in plete. Species are constantly being found in bees will be an essential element in achieving areas where they were previously unknown practical conservation. (MB, unpubl. data) National policy makers have adopted the There is an urgent need to train and create ecosystem services concept (Cork et al., employment opportunities for taxonomists and 2007), which will require the acquisition of for a large scale survey of Australia’s existing a great deal more experimental information bee fauna, in particular in view of the poten- about bee biology to provide a reasonable ba- tially important role for native bees as crop sis for decision making (Kremen et al., 2007). pollinators. Without such information, analysis of the ecosystem service is likely to be oversimpli- ACKNOWLEDGEMENTS fied (Cork et al., 2007) with undesirable con- sequences. However, with many undescribed We thank Rob Paxton and Mark Brown for their species and the overall lack of adequate iden- editorial role, and Remko Leijs for valuable discus- tification keys (Tab. I), the data that are needed sion and suggestions. 352 M. Batley, K. Hogendoorn

Diversité et statut de conservation des abeilles in- Schutzstatus der einheimischen Bienen Australiens digènes australiennes. erfordert die Ausbildung und die Einstellung von Bienentaxonomen. Apoidea / abeille indigène / Australie / protec- tion / taxonomie einheimische Bienen / Australien / Schutzstatus / Taxonomie

Zusammenfassung – Diversität und Schutz- status der einheimischen Bienen Australi- ens. Australien besitzt eine einzigartige Bienen- REFERENCES fauna, die sich durch einen hohen Anteil an Arten der Familie Colletidae und das Fehlen von Andre- AFD (2006), Cardale J.C. (2001) Updated by Walker nidae und Mellitidae auszeichnet. Aufgrund einer K.L. (2006) Hymenoptera: Apoidea, Australian geringen Anzahl an Kolonisierungsereignissen sind Faunal Directory, Australian Biological Resources viele Linien endemisch. Schätzungsweise 25 % Study, Canberra. http://www.environment.gov. der Arten sind noch unbeschrieben und 50 % der au/biodiversity/abrs/online-resources/fauna/afd/ Taxa bedürfen einer Revision. Insbesondere viele taxa/APOIDEA/checklist (accessed 12 February oligolektische Arten könnten übersehen worden 2009). und aufgrund fehlender Schutzmassnahmen be- droht sein. Des weiteren sind für insgesamt 57 % Anderson D. (2006) Improving lucerne pollination with leafcutter bees stage 2, Rural Industries der Arten keine Bestimmungsschlüssel verfügbar. Research and Development Corporation, Dies stellt ein schwerwiegendes Hindernis für Canberra. [online] http://www.rirdc.gov.au/ Untersuchungen der einheimischen Bienen durch reports/PSE/06-108.pdf (accessed on 30 January Laien oder Nichtextperten dar. Informationen zum 2009). Blütenbesuch und zum Nistverhalten gibt es nur für einige wenige Arten. Auld T.D. (2001) The ecology of the Rutaceae in Die vielfachen Bedrohungen der einheimischen the Sydney region of south-eastern Australia: Bienenfauna beinhaltet die Entfernung von poorly known ecology of a neglected family, Nistgelegenheiten und Futtersammelstellen, die Cunninghamia 7, 213–239. Ausbreitung eingeführter exotischer Pflanzen- Auld T.D., Denham A.J. (2006) How much seed re- arten und Klimaveränderungen. Grossflächige mains in the soil after a fire? Plant Ecol. 187, 15– Beseitigungen der natürlichen Vegetation für land- 24. wirtschaftliche Zwecke sind zwar im Rückgang, Bell M.C., Spooner-Hart R.N., Haigh A.M. (2006) die Veränderungen in der Zusammensetzung der Pollination of greenhouse tomatoes by the aus- Flora sind jedoch ein Grund zur Sorge. Diese tralian bluebanded bee Amegilla (Zonamegilla) Veränderungen rühren von der Beweidung durch holmesi (Hymenoptera:Apidae), J. Econ. Vieh und andere eingeführte Säugetiere her, sowie Entomol. 99, 437–442. durch den Ersatz einheimischer Pflanzen durch Bernhardt P. (1987) A comparison of the diversity, den- eingeführte Unkräuter. Letztere profitieren in sity and foraging behaviour of bees and wasps on ihrer Bestäbung nicht zuletzt von ausgewilderten Australian Acacia, Ann. Mo. Bot. Gard. 74, 42– oder beimkerten Honigbienenvölkern. Die direkte 50. Konkurrenz zwischen einheimischen Bienen und Honigbienen ist vermutlich variabel und abhängig Blanche K.R., Ludwig J.A., Cunningham S.A. (2006) von den jeweils verfügbaren Pflanzen als Nah- Proximity to rainforest enhances pollination and rungsquellen. fruit set in orchards, J. Appl. Ecol. 43, 1182–1187. Klimaveränderungen führen zu vermehrten Über- Bosch J., Kemp W.P. (2002) Developing and establish- schwemmungen und Buschfeuern und haben ing bee species as crop pollinators: the example als langfristige Konsequenz unvorhersehbare of Osmia spp. (Hymenoptera: Megachilidae) and Veränderungen in der floralen Abundanz und fruit trees, Bull. Entomol. Res. 92, 3–16. Phänologie zur Folge. All diese Faktoren be- Bray R.A. (1973) Characteristics of some bees of einflussen mit grosser Wahrscheinlichkeit die the family Megachilidae in Southeast Queensland Verteilung und Häufigkeit der einheimischen and their potential as alfalfa pollinators, J. Aust. Bienen. Einleitende Schritte zum Schutz der Entomol. Soc. 12, 99–102. einheimischen Bienenfauna könnten ihre Nutzung Cork S., Stoneham G., Lowe K. (2007) Ecosystem ser- als Bestäuber von Nutzpflanzen sein, sowie die vices and Australian natural resource management Anhebung des öffentlichen Bewusstseins über (NRM) futures: Paper to the Natural Resource den Schutz natürlicher Habitate. Der allgemeine Policies and Programs Committee (NRPPC) Mangel an Kenntnissen über die Taxonomie und and the Natural Resource Management Standing das Fehlen von Bestimmungsschlüsseln sind hierin Committee (NRMSC), Australian Government jedoch schwerwiegende Hinderungsgründe. Unsere Department of the Environment, Water, Heritage Fähigkeit des Monitoring und der Beurteilung des and the Arts, Canberra. Bees in Australia 353

Danforth B.N., Ji S. (2001) Australian Lasioglossum + T., Storey D., Poole L., Mallick S.A., Fitzgerald Homalictus form a monophyletic group: resolving N., Krirkpatrick J.B., Febey J., Harwood A.G., the “Australian Enigma”, Syst. Biol. 50, 268–283. Michaels K.F., Russell M.J., Black P.G., Emerson Danforth B.N., Sipes S., Fang J., Brady S.G. (2006) L., Visoiu M., Morgan J., Breen S., Gates S., The history of early bee diversification based on Bantich M.N., Desmachelier J.M. (2002) Extent five genes plus morphology, Proc. Natl. Acad. Sci. of invasion of Tasmanian native vegetation by USA 103, 5118–5123. the exotic bumblebee Bombus terrestris (Apoidea: Apidae), Aust. Ecol. 27, 162–172. Delaplane K.S., Mayer D.F. (2000) Crop pollination by bees, CABI Publishing, New York. Hogendoorn K., Steen Z., Schwarz M.P. (2000) Native Australian carpenter bees as a potential alternative Exley E.M. (1998) New Euryglossa (Euhesma) bees to introducing bumble bees for tomato pollination (Hymenoptera: Apoidea: Euryglossinae) associ- in greenhouses, J. Apic. Res. 39, 67–74. ated with the Australian plant genus Eremophila (Myoporaceae), Rec. West. Aust. Mus. 18, 419– Hogendoorn K., Gross C.L., Sedgley M., Keller 437. M.A. (2006) Increased tomato yield through pol- lination by native Australian Amegilla chloro- Exley E.M. (2004) Revision of the genus Dasyhesma cyanea (Hymenoptera: Anthophoridae), J. Econ. Michener (Apoidea: Colletidae: Euryglossinae), Entomol. 99, 828–833. Rec. West. Aust. Mus. 22, 129–146. Hogendoorn K., Coventry S.A., Keller M.A. (2007) Fellendorf M., Mohra C., Paxton R.J. (2004) Devasting ff Foraging behaviour of a blue banded bee, e ects of river flooding to the ground-nesting bee, Amegilla (Notomegilla) chlorocyanea Cockerell in Andrena vaga (Hymenoptera: Andrenidae), and its greenhouses: implications for use as tomato polli- associated fauna, J. Conserv. 8, 311–312. nators, Apidologie 38, 86–92. Gollan J.R., Batley M., Reid C.A.M. (2008) The Houston T.F. (1977) Nesting biology of three allodap- exotic bee Halictus smaragdulus Vachal, 1895 ine bees in the subgenus Exoneurella Michener (Hymenoptera: Halictidae) in the Hunter Valley, (Hymenoptera: Anthophoridae), Trans. R. Soc. S. N.S.W.: A new genus in Australia, Aust. Entomol. Aust. 104, 99–113. 35, 21–26. Houston T.F. (1989) Leioproctus bees associ- Gordon J., Davis L (2003) Valuing honeybee pollina- ated with Western Australian smoke bushes tion, Rural Industries Research and Development ( sp.) and their adaptations for Corporation, Canberra. [online] http://www.rirdc. / / / foraging and concealment (Hymenoptera: gov.au reports HBE 03-077.pdf (accessed on Colletidae: Paracolletini), Rec. West. Aust. Mus. 30 January 2009). 14, 275–292. ff Goulson D. (2003) E ects of introduced bees on native Houston T.F. (1992) Three new, monolectic species ecosystems, Annu. Rev. Ecol. Syst. 34, 1–26. of Euryglossa (Euhesma) from Western Australia Goulson D., Derwent L.C. (2004) Synergistic interac- (Hymenoptera: Colletidae), Rec. West. Aust. Mus. tions between an exotic honeybee and an exotic 15, 719–728. weed: pollination of Lantana camara in Australia, Houston T.F. (1993) Apparent mutualism between Weed Res. 44, 195–202. Verticordia nitens and V. aurea (Myrtaceae) and Griffin NRM Pty Ltd. (2004) Small steps for na- their oil-ingesting bee pollinators (Hymenoptera: ture: A review of progress towards the National Colletidae), Aust. J. Bot. 41, 369–380. Objectives and Targets for Biological Diversity Houston T.F. (2000) Native bees on wildflowers in Conservation 2001–2005, WWF Australia and Western Australia. A synopsis of bee visitation Humane Society International, Sydney. of wildflowers based on the bee collection of the Heard T.A. (1999) The role of stingless bees in crop Western Australian Museum, Special Publication pollination, Annu. Rev. Entomol. 44, 183–206. No. 2, Western Australian Insect Study Society, Perth. Hingston A.B., McQuillan P.B. (1998) Does the re- cently introduced bumblebee Bombus terrestris Kremen C., Williams N.M., Bugg R.L., Fay J.P., Thorp (Apidae) threaten Australian ecosystems? Aust. J. R.W. (2004) The area requirements of an ecosys- Ecol. 23, 539–549. tem service: crop pollination by native bee com- munities in California, Ecol. Lett. 7, 1109–1119. Hingston A.B., McQuillan P.B. (1999) Displacement of Tasmanian native megachilid bees by the re- Kremen C., Williams N.M., Aizen M.A., Gemmill- Herren B., LeBuhn G., Minckley R.L., Packer cently introduced bumblebee Bombus terrestris ff (Linaeus, 1758) (Hymenoptera: Apidae), Aust. J. L., Potts S.G., Roulston T., Ste an-Dewenter I., Zool. 47, 59–65. Vázquez D.P., Winfree R., Adams L., Crone E.E., Greenleaf S.S., Keitt T.H., Klein A.-M., Regetz J., Hingston A.B., Marsden-Smedley J., Driscoll D.A., Ricketts T.H. (2007) Pollination and other ecosys- Corbett S., Fenton J., Anderson R., Plowman tem services produced by mobile organisms: a C., Mowling F., Jenkin M., Matsui K., Bonham conceptual framework for the effects of land-use K.J., Ilowski M., McQuillan P.B., Yaxley B., Reid change, Ecol. Lett. 10, 299–314. 354 M. Batley, K. Hogendoorn

Lange R.T., Purdie R. (1976) Western myall (Acacia Praz C.J., Müller A., Dorn S. (2008) Specialised bees sowdenii) its survival prospects and management fail to develop on non-host pollen: do plants chem- needs, Aust. Rangeland J. 1, 64–69. ically protect their pollen? Ecology (Wash. DC) McDougall K., Kirkpatrick J.B. (1994) Conservation 89, 795–804. of lowland native grasslands in South-eastern Sattler P., Creighton C. (2002) Australian terres- Australia, World Wild Fund for Nature Australia, trial biodiversity assessment 2002, Department of Sydney. the Environment, Water, Heritage and the Arts, Matteson K.C., Ascher J.S., Langellotto G.A. (2008) Canberra. Bee richness and abundance in New York City ur- Schwarz M.P., Fuller S., Tierney S.M., Cooper S.J.B. ban gardens, Ann. Entomol. Soc. Am. 101, 140– (2006) Molecular phylogenetics of the exoneurine 150. allodapine bees reveal an ancient and puzzling dis- Michener C.D. (1965) A classification of the bees of persal from Africa to Australia, Syst. Biol. 55, 31– the Australian and South Pacific regions, Bull. 45. Am. Mus. Nat. Hist. 130, 1–362. Simpson S.R., Gross C.L., Silberbauer L.X. (2005) Michener C.D. (2000) The bees of the world, John Broom and honeybees in Australia: An alien liai- Hopkins University Press, Baltimore. son, Plant Biol. 7, 541–8. Morton S.R., Short J., Barker R.D. (1995) Refugia Steffan-Dewenter I., Schiele S. (2008) Do resources or for biological diversity in arid and semi-arid natural enemies drive bee population dynamics in Australia, Paper No. 4, Biodiversity Unit, fragmented habitats? Ecology 89, 1375–1387. Australian Government Department of the Stout J., Morales C.L. (2009) Ecological impacts of in- Environment, Water, Heritage and the Arts, vasive alien species on bees, Apidologie 40, 388– // Canberra. [online] http: www.environment. 409. gov.au/publications/series/paper4/index.html (accessed on 30 January 2009). Tomassi D., Miro A., Higo H.A., Winston M.L. (2004) Bee diversity and abundance in an urban setting, Murray T.E., Kuhlmann M., Potts S.G. (2009) Can. Entomol. 136, 851–869. Conservation ecology of bees: populations, species and communities, Apidologie 40, 211– Walker K.L. (2008) Carder bee (Afranthidium 236. (Immanthidium) repetitum) pest and diseases image library. [online] http://www.padil.gov.au Paton D.C. (1996) Overview of the feral and managed (accessed 30 January 2009). honeybees of Australia: distribution, abundance, extent of interactions with native biota, evidence Zayed A. (2009) Bee genetics and conservation, of impacts and future research, Australian Nature Apidologie 40, 237–262. Conservation Society, Melbourne. Zayed A., Packer L., Grixti J.C., Ruz L., Owen R.E., Paini D.R. (2004) Impact of the introduced honey bee Toro H. (2005) Increased genetic differentiation in (Apis mellifera)(Hymenoptera: Apidae) on native a specialist versus a generalist bee: implications bees: a review, Aust. Ecol. 29, 399–407. for conservation, Conserv. Genet. 6, 1017–1026.