Humanity has long been fascinated by animals with apparently unfavorable lifestyles []. Nesting habits are especially important because they can limit where organisms live, thereby driving population, community, and even ecosystem dynamics []. The question arises, then, why bees nest in active termite mounds [] or on the rim of degassing volcanoes, seemingly preferring such hardship []. Here, we present a new bee species that excavates sandstone nests, Anthophora (Anthophoroides) pueblo Orr (described in Supplemental Information, published with this article online), despite the challenges already inherent to desert life. Ultimately, the benefits of nesting in sandstone appear to outweigh the associated costs in this system.

The biology and description of a new species of African Thyreus, with life history notes on two species of Anthophora (Hymenoptera: Anthophoridae).

Main Text

Figure 1 Distribution, study sites, and substrate use of Anthophora pueblo. Show full caption Collection and nest study sites are indicated, and areas where sandstone is dominant are shaded. 83% of collection sites (35/43) were within 1 km of sandstone-dominated areas, all were within 10 km, and smaller patches of sandstone are likely present even closer to these collection events. Inset frames include: Site 1, 1980 sandstone sample collection site, where the aggregation still persists, also demonstrates the avoidance of hardened patina in >90% of observed nests; Site 3, nests within an Ancestral Puebloan cliff dwelling wall; and Site 6, preference for water-damaged, weaker areas, even in silt. All sites had minimally intermittent water sources, which may provide the liquid this species is believed to use for excavation (see also Figure S1 and Movies S1 and S2 ). Almost forty years ago in Utah’s San Rafael Desert, Frank Parker discovered bees nesting in sandstone at two sites, excavated sandstone blocks, and reared the bees within to emergence ( Figure 1 and Supplemental Information). Hidden away in a museum until 2015, the nests of this new species waited to be unearthed. Now, after discovering five new nesting sites, ranging from Ancestral Puebloan sandstone cliff dwellings and natural formations to vertical silt deposits, we better understand why these xeric bees nest in sandstone.

It was first necessary to confirm that Anthophora pueblo actually prefers nesting in sandstone. We found that Anthophora pueblo uses sandstone up to a hardness threshold, above which it will apparently excavate other substrates. Although sandstone is present where bees also use silt (Sites 6, 7), that sandstone is nearly twice as hard as the average sandstone used elsewhere (Schmidt Indices: 22.3 versus 12.8, respectively; Supplemental Information). At the other sites with weaker sandstone (1, 5, 7), bees never used alternative substrates and locally preferred weaker sandstone (average Schmidt Index of 13.7 versus 33.9 in unused portions; U = 1; p < 0.05). X-ray diffraction analyses of mineral composition at Site 1 help explain these hardness differences (Supplemental Information). The weaker, nested areas had less quartz and more clay (nontronite, illite in places without nests), which likely contributed to sandstone softness ( Figure S1 ). It is no surprise, given bee preferences, that all collection events occurred near sandstone ( Figure 1 ).

2 Stephen W.P.

Bohart G.E.

Torchio P.F. The Biology and External Morphology of Bees, with a Synopsis of the Genera of Northwestern America. This species’ preference for sandstone becomes particularly puzzling when considering the associated costs. As sandstone is harder than other substrates bees excavate (e.g., sand or soil), higher energy and time costs are expected. Mandible wear is consistently seen in older females, a consequence of excavation that likely limits their further use. The preference for softer sandstone also appears to result in high nest density that may cause nest site competition []. These aggregations may even attract parasites, as evidenced by them outnumbering Anthophora pueblo (>3:1) in one sandstone sample ( Table S1 ).

5 Cane J.H. A native ground-nesting bee (Nomia melanderi) sustainably managed to pollinate alfalfa across an intensively agricultural landscape. 6 Danforth B.N. Emergence dynamics and bet hedging in a desert bee, Perdita portalis. Despite the costs of sandstone nesting, the persistence of this behavior in Anthophora pueblo suggests offsetting benefits; indeed, Site 1 represents the longest-lasting solitary bee nesting aggregation ever documented, aside from Nomia melanderi beds where managers control parasites to maintain population health []. Benefits of sandstone’s durability that may explain this include increased structural integrity and tunnel reuse by offspring. A related benefit is the ability to delay emergence and instead stay in the protected nests for up to at least four years (Supplemental Information). Delayed emergence is a bet-hedging strategy for avoiding years with poor floral resources, especially useful in xeric areas prone to drought; absence of precipitation may have caused sample specimens to delay emergence []. However, each additional year of delay entails added risk of destruction by erosion or flash floods. The superior protection afforded by sandstone likely reduces such damage.

2 Stephen W.P.

Bohart G.E.

Torchio P.F. The Biology and External Morphology of Bees, with a Synopsis of the Genera of Northwestern America. 7 Girvan M.S.

Bullimore J.

Pretty J.N.

Osborn A.M.

Ball A.S. Soil type is the primary determinant of the composition of the total and active bacterial communities in arable soils. 8 Wynns A.A.

Jensen A.B.

Eilenberg J. Ascosphaera callicarpa, a new species of bee-loving fungus, with a key to the genus for europe. 9 Torchio P.F.

Bosch J. Biology of Tricrania stansburii, a meloid beetle cleptoparasite of the bee Osmia lignaria propinqua (Hymenoptera: Megachilidae). Nesting in sandstone may also help Anthophora pueblo manage threats like pathogens or parasites []. Substrate affects microbial community composition [], and sandstone, with less organic matter, may have more microbes that subsist on photosynthesis (e.g., cyanobacteria). One might, therefore, expect lower microbe incidence in elevated, sandstone nests. This was supported at Site 1, as a fallen sandstone block on the ground experienced significantly higher microbial invasion than intact, elevated sandstone (79% versus 28% of Anthophora cells, respectively; p<0.0001). Although some microbes likely invaded post-mortem, an unknown Ascosphaera (chalkbrood) found in dead Anthophora pueblo larvae appears truly pathogenic (Tripodi, pers. comm.). Known to cause significant mortality in some bees, this is the first record of this fungus in a non-social, non-megachilid bee []. Sandstone may also hinder parasites that usurp nests, such as the meloid beetle Tricrania stansburii ( Table S1 ). While prevalent in the 1980 sample, only 6/69 Tricrania successfully emerged, the rest having died in nest cells. Sandstone may, thus, inhibit parasite buildup across years, as the cell closure is generally too hard for Tricrania to breach in harder substrates [].

Though apparently detrimental to some of the 20 known nest associates of Anthophora pueblo ( Table S1 ), others may benefit from inhabiting sandstone. Two parasites delayed their emergences, including the first confirmed record for parasitic bees (Xeromelecta californica; Table S1 ). Just as Anthophora pueblo benefits from waiting for sufficient bloom, so too should parasites benefit from synchronizing with host activity. Associates likely also benefit from the durability of sandstone and its potential effects on microbes and parasites. Through excavating, Anthophora pueblo creates a novel habitat. Conversely, by avoiding excavation, associates reap sandstone’s benefits while avoiding most costs.

The evolutionary drive to minimize costs raises a new question. Although Anthophora pueblo reusing old nests avoid excavation costs, as associates do, excavators cannot. How did this behavior evolve? The answer may lie in the offspring, which could increase the indirect fitness of relatives through trans-generational trade-offs between the costs of excavation versus competition. If existing nests are abundant, bees can provision more cells without excavating. However, alongside the increasing population, nest site competition and its costs would increase for each generation. The resultant selection for excavation could be augmented if few females colonize new sites and their offspring are unusually closely-related, through indirect fitness from offspring, relatives, and their offspring. The bees may even cooperate, as is suggested by observations of females aggressively chasing parasites from nest aggregations, rather than defending only their own nests. Ultimately, the high investment of excavators may yield unexpected evolutionary dividends. In balancing the costs and benefits of its lifestyle in relation to its xeric environment, Anthophora pueblo has pioneered a suitable niche between a rock and the desert, a hard place to live.