The Australian endemic bee, Pharohylaeus lactiferus (Colletidae: Hylaeinae) is a rare species that requires conservation assessment. Prior to this study, the last published record of this bee species was from 1923 in Queensland, and nothing was known of its biology. Hence, I aimed to locate extant populations, provide biological information and undertake exploratory analyses relevant to its assessment. Pharohylaeus lactiferus was recently rediscovered as a result of extensive sampling of 225 general and 20 targeted sampling sites across New South Wales and Queensland. Collections indicate possible floral and habitat specialisation with specimens only found near Tropical or Sub-Tropical Rainforest and only visiting Stenocarpus sinuatus (Proteaceae) and Brachychiton acerifolius (Malvaceae), to the exclusion of other available floral resources. Three populations were found by sampling bees visiting these plant species along much of the Australian east coast, suggesting population isolation. GIS analyses used to explore habitat destruction in the Wet Tropics and Central Mackay Coast bioregions indicate susceptibility of Queensland rainforests and P. lactiferus populations to bushfires, particularly in the context of a fragmented landscape. Highly fragmented habitat and potential host specialisation might explain the rarity of P. lactiferus. Targeted sampling and demographic analyses are likely required to thoroughly assess the status of this species and others like it.

Conservation, extinction risk, fragmentation, Hylaeinae, invertebrate conservation, Queensland, wildfire, rainforest

The greatest threats to ecosystems and species worldwide are habitat loss, fragmentation and degradation (Vie et al. 2009). Australia has already cleared over 40% of its forests and woodlands since European colonisation, leaving much of the remainder fragmented and degraded (Bradshaw 2012). The vast majority of clearing has occurred on freehold and leasehold land and for animal agriculture (Evans 2016). In particular, Queensland is a contemporary land-clearing hotspot and is responsible for more than half of all land-clearing in Australia over the past four decades (Evans 2016). It is a failing of state and federal government policy and regulation that land clearing in Queensland continues at rates that should be of concern both nationally and internationally (Reside et al. 2017).

Despite the ecological importance of Australian native bees, we know very little about their biology (Batley and Hogendoorn 2009) or conservation status. North Queensland hosts high species richness and endemism (Crisp et al. 2001; Orme et al. 2005; Hurlbert and Jetz 2007) and several bee genera that are found nowhere else in Australia (Houston 2018; Smith 2018). These restricted bee genera include: Ctenoplectra Kirby (Apidae: Apinae), Nomada Scopoli (Apidae: Nomadinae), Mellitidia Guérin-Méneville (Halictidae: Nomiinae), Reepenia Friese (Halictidae: Nomiinae), Patellapis Friese (Halictidae: Halictinae) and Pharohylaeus Michener (Colletidae: Hylaeinae).

Pharohylaeus has only two described species: P. papuaensis Hirashima & Roberts in Papua New Guinea and P. lactiferus (Cockerell) in Australia (Houston 1975; Hirashima and Roberts 1986). Both species are relatively large (9–11 mm), robust, mostly black with distinctive white facial and body markings, and have the first three tergal segments enlarged and enclosing the others. The former is known only from two females which were collected on Syzygium aqueum (Burm.f.) Alston (Myrtaceae) in 1982 (Hirashima and Roberts 1986). No published records of P. lactiferus have been made since the third of January 1923, when three males were collected in the Atherton Tablelands; in May of 1900 a male and a female were collected in Mackay while another female was collected in Kuranda prior to 1910 (Cockerell 1910; Houston 1975). However, the collection localities of these specimens are imprecise and no biological data were recorded.

Due to the dearth of biological information on P. lactiferus prior to this study, I aimed to locate extant populations and contribute biological information as part of a broader bee survey. Because of this, much of what follows are exploratory analyses of the potential risks for P. lactiferus and suggestions for future research. Hence, I undertook a series of post-hoc analyses in order to provide insights into the biology, ecology and potential extinction risks associated with P. lactiferus. I provide insights into the circumstances of the rediscovery of P. lactiferus and what is now known of its floral and habitat associations. I also explore spatial data relating to P. lactiferus (vegetation association, potential fire risks and occurrences) and my sampling methods (for potential biases). The possible floral and habitat specialisation along with the rarity of P. lactiferus raises concerns about its conservation status. I further highlight the need for preservation of remnant vegetation and better arthropod-diversity monitoring, particularly for at-risk and phylogenetically important species.

Despite my extensive non-targeted and targeted sampling as well as bee collection records on the Atlas of Living Australia, P. lactiferus records remain rare. Apparent habitat specialisation to TSTRs and few associated floral taxa (S. sinuatus and B. acerifolius) might explain the rarity of P. lactiferus. However, in many cases I found P. lactiferus difficult to catch due to the height of the associated plant species (of the trees that I sampled, flowers were between 1 m and 13 m high) and the bees’ quick flight (Suppl. material 1: Appendix). It is possible that P. lactiferus is a naturally rare species that is not threatened. But, why at least two early collectors sampled P. lactiferus on three separate occasions prior to 1924 (Houston 1975) and no published records have been made in the years since, despite a greater sampling effort (Fig. 2), is both unclear and of concern.

The occurrence of host plant species could limit suitable habitat for P. lactiferus. For example, the persistence of a P. lactiferus population in any one rainforest could require several host plant species to provide food throughout their activity period. From current and historical collections, we know that P. lactiferus is active at least between November and May. This could indicate a long flight period, bivoltinism or, like many other tropical bee species (e.g., (ALA 2019; Dorey et al. 2019)), activity could be year-round. Additionally, as many hylaeines nest in preformed holes (Almeida 2008; Houston 2018), P. lactiferus might require very specific nesting substrates (Hearn et al. 2019). Nesting substrate could further be limited to certain plant species, and by certain stem-borers that pre-excavate potential nests (Dew and Schwarz 2013; Houston 2018). Habitat destruction and fragmentation might also limit the persistence of the required species in fragments (Suppl. material 1: Appendix). These factors might be particularly relevant to P. lactiferus, which was only found within ~200 m of TSTR, suggesting a low foraging and dispersal distance (Suppl. material 1: Appendix).

That bees use S. sinuatus and B. acerifolius might be unexpected for two primary reasons. Firstly, both plant species exhibit a pollination syndrome that is associated with birds (e.g., they are bright red) (Nicolson and Van Wyk 1998; Williams and Adam 2010; Shrestha et al. 2013). Bee vision is shifted towards ultraviolet wavelengths and they are thought to not perceive red wavelengths (Dyer et al. 2015); although, this is not always the case (Peitsch et al. 1992) and insect visual perception is complex (Horridge 1998). It is possible that the flowers of S. sinuatus and B. acerifolius have ultraviolet, or similar, markings or produce olfactory cues that attract bees. That at least ten bee species across eight genera were foraging on B. acerifolius could indicate that this plant is not exclusively bird-pollinated (Suppl. material 2: Table S1). Hylaeinae bees were the primary visitors of B. acerifolius during observations (Suppl. material 2: Table S1) which could indicate phylogenetically conserved traits that allow the use of flowers that exhibit bird-pollination syndromes (e.g., pollen specialisation or red-shifted vision). Secondly, Guymer (1988) reported that B. acerifolius lacks nectaries. While I did not observe bees inside flowers due to the height of trees, I did observe bees ‘drinking’ from flowers of the related B. populneus (Schott & Endl.) R.Br., which Guymer (1988) also reports as lacking nectaries. Melittologists might avoid sampling plants that exhibit bird-pollination syndromes and this could bias their collections. The foraging preferences of P. lactiferus require further study, likely with a particular focus on plants exhibiting bird-pollination syndromes (e.g., Alloxylon pinnatum (Maiden & Betche) P.H.Weston & Crisp, Castanospermun australe A.Cunn. ex Mudie or Erythrina vespertilio Benth.) or even on canopy-flowering plants in general (Roubik 1993).

In the bioregions that P. lactiferus has been found, this major vegetation subgroup has undergone habitat destruction and fragmentation since European colonisation (Suppl. material 1: Appendix) (Bradshaw 2012). Although Queensland’s Wet Tropics have largely been protected from clearing in contemporary times, like much of the state, habitat fragmentation remains a major conservation concern (Tucker 2000). Additionally, three of four rainforest vegetation types (including TSTR) burnt every year between 1988 and 2020 (for which data are available; Suppl. material 1: Appendix). While there was no significant change over time in the area of rainforest burnt during that period, the 2019–2020 bushfire season burnt a greater area than in any year prior for each rainforest type (Suppl. material 1: Appendix).

To monitor and assess the conservation status of each species we require an understanding of their biology and targeted sampling. Data deficiency for rare species raises concerns that other rare or specialist species could become extinct before being discovered, leaving no opportunity to conserve those taxa. We must increase biomonitoring, particularly of diverse invertebrate fauna to assess and protect such taxa worldwide. Additionally, increasing institutional investment to digitise collections would vastly increase the research utility of online databases and potentially allow us to differentiate rare from threatened taxa.

Future research should aim to increase our understanding of the biology, ecology and population genetics of P. lactiferus. This work could use targeted seasonal sampling throughout the year at sites where P. lactiferus is known to occur, providing insights into phenology and host plant species. Future studies could also use trap-nests at various heights from the ground and targeted searches to uncover nesting requirements and inform conservation management (Roubik 1993; Sutherland et al. 2010). These data, along with an expanded a priori sampling regime, should allow accurate implementation of species distribution models to uncover other potential populations or translocation sites. To determine if P. lactiferus is threatened (undergone population declines in the recent past) or simply rare (stable population in the recent past), genetic data could be used to examine past demographies. Additionally, genetic data for each population could allow examination of population isolation. Such research will be invaluable to assess the conservation status of P. lactiferus and provide an exemplar for the assessment of other poorly-studied and threatened bee taxa.

Despite extensive sampling undertaken during this study and from publicly available records, P. lactiferus remains poorly collected and little is known of its biology. Pharohylaeus lactiferus has only been collected on two plant species (S. sinuatus and B. acerifolius), to the exclusion of other available resources. Thus far, only males have been collected on S. sinuatus. These collections might indicate floral specialisation, potentially on plants that exhibit bird-pollination syndromes.

Many of the analyses undertaken here are exploratory and this must be considered when making conclusions. However, it is important for likely issues to be raised in order to inform future research and conservation efforts. To these ends, I make the following remarks. Pharohylaeus lactiferus could be a floral- and habitat-specialist bee. The absence of P. lactiferus collections since 1923, despite far-greater sampling effort prior to this study, raises concerns about its conservation status. Habitat destruction and fragmentation might have acted synergistically with the floral- and habitat-specialisation of P. lactiferus to explain its rarity. However, collection habits of melittologist (e.g., possible avoidance of plants with bird-pollination syndromes) and the height of known associated plants might make possible declines difficult to confirm. Regardless, known populations of P. lactiferus remain rare and susceptible to habitat destruction (e.g., from changed land use or stochastic events such as fires; Suppl. material 1: Appendix).

I would like to thank Olivia K. Davies, Michael P. Schwarz and Mark I. Stevens for proofing early versions of the manuscript. I further thank Lori Lach, Jack Neff, Terry Houston and four anonymous reviewers for their insightful comments on the manuscript that led to its improvement. I would also like to thank Erinn P. Fagan-Jeffries and Peter Rühr for their company during field work. I would finally like to thank the funders of this research (Holsworth Wildlife Research Endowment, Playford Trust PhD Scholarship and AJ and IM Naylon PhD Scholarship) that support and promote the research of many young scientists. This work was carried out under the Queensland national parks research permit number PTU18-001277-1 and the New South Wales National Parks & Wildlife Service scientific licence number SL102137.