Biological Conservation 144 (2011) 2631–2636 Contents lists available at ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon Predicted fates of ground-nesting bees in soil heated by wildfire: Thermal tolerances of life stages and a survey of nesting depths ⇑ James H. Cane a, , John L. Neff b a USDA-ARS Pollinating Insect Research Unit, Utah State University, Logan, UT 84322, United States b Central Texas Melittological Institute, 7307 Running Rope, Austin, TX 78731, United States article info abstract Article history: Periodic wildfire defines plant community composition and dynamics in many of the world’s semi-arid Received 17 March 2011 biomes, whose climates and floras also favor wild bee diversity. Invasive flammable grasses, deforesta- Received in revised form 15 July 2011 tion, historical fire suppression and human ignition are increasing fire frequency and intensifying its Accepted 16 July 2011 severity, as well as introducing fire to previously fireproof biomes. In many of these habitats, bees are Available online 11 August 2011 key pollinators. Many, often most of the solitary bee species and individuals in these biomes nest under- ground (so-called ‘‘mining’’ bees). To evaluate their susceptibility to fire, we tested heat tolerances of Keywords: bees’ four life stages using an experimental design that mimicked heat conduction dynamics of natural Apiformes soils. All life stages survived heating of up to 45 °C for 27 min, but none survived heating at 54 °C for Apoidea Pollinator 9 min; the pupal stage survived best. At near-lethal temperatures, more prolonged heating caused more Fire mortality. These data were related to published studies of heat penetration depths in soil during fire and an exhaustive compilation of published nesting depths reported for mining bees. We conclude that a small fraction (9%) of the shallowest-nesting mining bee species is likely to die from soil heating by wild- fire. Among these, ground-nesting megachilids (Osmia, Megachile) will be most vulnerable, owing to their shallow horizontal nests. Because mining bees prevail in most biomes of the temperate zone, any vege- tation rehabilitation efforts should therefore expect that bee communities will largely survive the imme- diate effects of wildfire, and therefore will need pollen and nectar resources in the year(s) after fire. Published by Elsevier Ltd. 1. Introduction biomes, as well as other ecoregions of the world (Brooks et al., 2004). A prime example is annual Eurasian cheatgrass, Bromus tec- Fire is a major ecological factor in many terrestrial biomes, par- torum L., that has escaped into the American sage-steppe, where it ticularly grasslands, savannahs and Mediterranean-climate shrub- greatly increases the horizontal continuity of flammable vegetation lands (Bond and van Wilgen, 1996; DeBano et al., 1998). The (Chambers et al., 2007). These altered wildfire regimes are likely to importance of fire in these semi-arid biomes is readily observed intensify inasmuch as global warming prolongs growing seasons when fire is suppressed. Historically, many of these ecosystems and magnifies summer heat and droughts (Westerling et al., 2006). burned periodically, often with fires of relatively low intensity Bees, particularly non-social species, are the most diverse, abun- (sensu DeBano et al., 1998). Many plants in these systems have dant, and dominant pollinator group in these arid and semi-arid bio- adaptations that enable them to cope with these low intensity mes (Michener, 2007) that experience periodic fires (Bond and van cooler fires (Bond and van Wilgen, 1996). Wilgen, 1996). Fire can impact bee faunas in several direct ways. In Over the past century, fire intensities and return frequencies the short term, flames of surface fires scorch flowering forbs and have increased in many biomes. In many forests of North America, shrubs, their surface roots (Neary et al., 1999) and any current Europe and Australia, for instance, surface fuels have accumulated bloom; crown fires can consume bee-pollinated flowering trees as an unintended consequence of many decades of effective fire (e.g., Australian Eucalyptus). Fire also consumes many potential nest suppression policies (Neary et al., 1999; Pyne et al., 1996). Addi- sites (and residents) of twig- and cavity-nesting bees. Indirectly, fire tionally, invasions of flammable alien plants are fueling more in- changes the availability of resources for bees, often for the better tense and frequent fires across some semi-arid North American (e.g., Potts et al., 2003). In the growing seasons following a fire, a pulse of more diverse and abundant bloom sometimes (Seefeldt et al., 2007; Wrobleski and Kauffman, 2003) but not always (Platt ⇑ Corresponding author. Address: USDA Bee Biology Lab, Utah State University, Logan, UT 84322-5310, United States. Tel.: +1 435 797 3879; fax: +1 435 797 0461. et al., 1988) results, as flowering plants resprout or germinate to E-mail addresses: [email protected] (J.H. Cane), [email protected] take advantage of habitats opened by fire. There also may be an in- (J.L. Neff). crease in water availability and a surge of nutrients that leach from 0006-3207/$ - see front matter Published by Elsevier Ltd. doi:10.1016/j.biocon.2011.07.019 2632 J.H. Cane, J.L. Neff / Biological Conservation 144 (2011) 2631–2636 the ash (Chambers et al., 2007; Christensen and Muller, 1975), again in large numbers and are difficult to excavate and transport un- to the benefit of germinating or resprouting flowering plants and harmed. We chose two species of Megachilidae, Osmia lignaria Say their bee pollinators. and Megachile rotundata (Fab.). Both species are readily available A few studies have characterized bee communities’ responses to and have familiar life history parameters (Bosch and Kemp, 2001; fire (Campbell et al., 2007; Grundel et al., 2010; Potts et al., 2003). Pitts-Singer and Cane, 2011). Moreover, these two genera include They invariably report bee faunas to be present, along with more other species that, instead of the more familiar cavity-nesting habit, bloom, but the fires studied have been small in size (e.g., 10 ha, nest shallowly underground (Cane et al., 2007; Eickwort et al., 1981). Campbell et al., 2007). Hence, it is impossible to know whether We measured survival during soil heating in assays that mimicked the bees sampled were residents (or their descendents) that sur- fire heating of soil so that responses of these two cavity-nesting spe- vived the fire or were recent colonists from unburned surround- cies would be relevant to their shallow-nesting congenerics and ings. Larger-bodied species could even fly in from beyond the fire ground-nesting bees in general. perimeter on their foraging rounds; for instance, both Nomia mel- anderi (Cane, pers. obs.) and bumblebees (Osborne et al., 2008) 2.2.1. Adults have been seen foraging at distances of 1.5 km or more from their Loose cocoons containing adult male O. lignaria from northern nests. Our study was motivated by a need of land managers to Utah were overwintered at 4 °C until mid-March. These were X- anticipate the match between post-fire pollination services and rayed to find and discard the few cells that were parasitized, dis- the choice of wildflowers to be seeded back into large wildfires, eased, or with pre-pupae; all live individuals still had fat body re- where distances from edge habitat are substantial. Seeding pollina- serves (clear zone in X-ray negatives). Immediately prior to tor-dependent wildflowers into places where pollinators have been experimentation, cocoons were warmed to 9 °C for 18 h, a compro- extirpated could be a costly mistake. mise to lessen thermal shock but without eliciting emergence of Wildfires are most likely late in the dry season due to various this early spring bee. Following an experiment, cocoons were combinations of heat, drought, summer lightning and dry vegeta- placed individually in gel caps and incubated at 24 °C for a week tion (Pyne et al., 1996). In the temperate zone, this typically is while daily checking for emergence of live adults. the season that follows the one of flowering and bee foraging. Therefore, the immature stages in their natal nests are the ones 2.2.2. Immatures most likely to experience fire’s heat. Adult bees may be able to es- Loose nest cells containing pre-pupae (post-feeding larvae) of cape fires through flight, but their nests with eggs, larvae, pupae M. rotundata (mixed sexes) from Canada were overwintered at and pre-emergent adults are immobile and thus susceptible to fire. 4 °C until early April. These were X-rayed to find and discard the Nest residents may die from lethal substrate heating unless the few cells that were parasitized, diseased or empty. To elicit pupa- nests are adequately insulated. tion, cells were incubated at 30 °C for 12 days prior to experimen- We experimentally subjected live bee eggs, larvae, pupae and tation. Ten cells were dissected to confirm that pre-pupae had pre-emergent adults to incremental heat intensities and durations transformed to young pupae for experimental use. Following an using moist sand substrates and other protocols designed to mimic experiment, cocoons were returned to the incubator and, over soil heating by fire via conduction. We also compiled a first-ever 28 days, monitored daily for adult emergence. database of bee nesting depths for 449 ground-nesting bee species In July, a nesting population of M. rotundata was started in Lo- gleaned from the literature and our own unpublished records. We gan, Utah using standard polystyrene foam nesting blocks with pa- used this database to estimate the proportion of ground-nesting per straw liners inserted into the holes. Adults had access to alfalfa bee species that might be susceptible to lethal soil temperatures (Medicago sativa L.) and other flowers.