Abstract Gregarious nesting behavior occurs in a broad diversity of solitary bees and wasps. Despite the prevalence of aggregative nesting, the underlying drivers and fitness consequences of this behavior remain unclear. I investigated the effect of two key characteristics of nesting aggregations (cavity availability and progeny density) on reproduction and brood parasitism rates in the blue orchard bee (Osmia lignaria Say) (Hymenoptera: Megachilidae), a solitary species that nests gregariously and appears to be attracted to nesting conspecifics. To do so, I experimentally manipulated nest cavity availability in a region of northern Utah with naturally occurring populations of O. lignaria. Nest cavity availability had a negative effect on cuckoo bee (Stelis montana Cresson) (Hymenoptera: Megachilidae) parasitism rates, with lower parasitism rates occurring in nest blocks with more available cavities. For both S. montana and the cleptoparasitic blister beetle Tricrania stansburyi Haldeman (Coleoptera: Meloidae), brood parasitism rate was negatively correlated with log-transformed O. lignaria progeny density. Finally, cavity availability had a positive effect on male O. lignaria body weight, with the heaviest male progeny produced in nest blocks with the most cavities. These results suggest that cavity availability and progeny density can have substantial effects on brood parasitism risk and reproduction in this solitary bee species. Spatially aggregated nesting is common among many solitary bees and wasps. Although the majority of solitary hymenopterans provision nests individually, females often select nest locations in close proximity to conspecifics (Michener et al. 1958, Wcislo 1992). In more extreme cases, naturally occurring aggregations of ground-nesting species can reach upward of several hundred thousand individuals (Rozen and Buchmann 1990, Cockerell 1933). Although aggregative nesting appears to be fairly ubiquitous among solitary hymenopterans, the factors driving this behavior and the consequences for reproduction are unclear. Several hypotheses have been proposed to explain the prevalence of gregarious nesting in solitary bees and wasps (reviewed in Rosenheim 1990). First, aggregations may result from limitations in suitable nest sites and/or substrate. Ground-nesting species that prefer a specific soil type, for instance, may exhibit spatially clumped nesting in regions where that soil type occurs (Potts and Willmer 1997). However, many solitary hymenopterans nest gregariously despite an abundance of available nest sites (Michener et al. 1958, Bosch 1994, Tepedino and Torchio 1994, Eickwort et al. 1977). Limitations in other resources, such as patchy floral distributions, may also result in aggregated nesting. Zurbuchen et al. (2010) reported a significant decrease in the number of brood cells produced by two megachilid bee species (Hoplitis adunca (Panzer) [Hymenoptera: Megachilidae] and Chelostoma rapunculi (Lepeletier) [Hymenoptera: Megachilidae]) with increasing distance to floral resources, presumably because females had to expend additional energy collecting pollen and nectar. Nesting females may therefore be more likely to aggregate near resource patches, particularly in areas with high spatial heterogeneity. Aggregative behavior may also reduce the time spent searching for a nest site and improve nesting efficiency. The search costs associated with locating new nest sites can be substantial (Brockmann 1979, Klein et al. 2004) and there may be strong selective pressure to increase the efficiency of these energetically expensive activities (Potts and Willmer 1997). To reduce search time, females may rely on aggregations of nesting conspecifics as an indicator of microhabitat suitability (Eickwort et al. 1977). A related strategy that may contribute to the prevalence of aggregations is the tendency to nest near emergence sites (‘natal philopatry’, Yanega 1990). For instance, after dispersing and spending 8–11 months in diapause, the primitively eusocial sweat bee Halictus rubicundus (Christ) (Hymenoptera: Halictidae) returns to its emergence site and digs a burrow within 50 cm of its natal nest (Yanega 1990). This behavior may evolve as a risk avoidance strategy in which females remain at a known nesting site rather than search for a new, potentially untested one (Rosenheim 1990). In addition to improving nesting efficiency, aggregative behavior may reduce parasitism risk. In nesting aggregations of the digger wasp Crabro cribrellifer (Packard) (Hymenoptera: Sphecidae), the average number of parasitic sarcophagid flies present at nest sites increased as host nest density increased (Wcislo 1984). However, the rate of nest parasitism declined with increasing host density, suggesting that the probability of an individual being parasitized is lower in locally dense clusters of conspecifics (‘selfish herds’, Hamilton 1971, Wcislo 1984). Several potential factors may result in reduced parasitism rates in nesting aggregations. First, parasitoids may be physically limited by their oocyte maturation rate and/or by the handling time required to parasitize individual hosts (Rosenheim 1990). The egg limitation mechanism may be more likely in systems where parasitoid recruitment to host aggregations is limited, the number of hosts per aggregation is greater than the total number of mature parasitoid eggs at any given time, and the parasitoid’s ability to adjust its oocyte maturation rate is constrained. The handling time mechanism is more likely if parasitoid recruitment to host aggregations is limited and the time to successfully identify and parasitize a host is non-zero. Second, host vigilance and/or nest defense in aggregations may reduce parasitism risk. In the gregarious solitary bee species Anthophora edwardsii Cresson (Hymenoptera: Anthophoridae), for instance, multiple females will attack an invading parasite and drive it away from the aggregation (Thorp 1969). In order for this mechanism to be in effect, hosts must be able to recognize the parasite or parasitoid. Finally, host aggregations may cause a decline in parasitism due to the ‘encounter-dilution effect’. This effect may occur if the probability a searching parasite detects a host aggregation does not increase in proportion to group size and the parasite does not attack proportionally more hosts in larger aggregations (Mooring and Hart 1992). In solitary bees and wasps, several related features of nesting aggregations may influence reproduction and brood parasitism risk. The number of pre-existing nest cavities (cavity availability) is associated with changes in the relative abundance and community structure of wild cavity-nesting bees (Potts et al. 2005). The number of cavities in an aggregation may also affect parasitism risk, particularly for hymenopteran parasitoids and cleptoparasites that use visual cues to locate host nests (Rosenheim 1987, Van Nouhuys and Kaartinen 2008). The cuckoo bee Stelis montana Cresson (Hymenoptera: Megachilidae), for instance, is visually attracted to host nest sites with larger surface areas and appears to recognize nest cavities as interruptions in the surface (Torchio 1989a). A related characteristic of nesting aggregations that can also affect brood parasitism risk is the number of progeny produced per cavity (progeny density). Unlike cavity availability, which is a physical attribute of a nest site, progeny density is a biological characteristic that can provide a direct measure of host availability and the spatial concentration of brood cells. There are numerous examples in the literature in which parasitism rate in solitary hymenoptera is density dependent (Freeman and Parnell 1973, Freeman and Taffe 1974, Strohm et al. 2001), inversely density dependent (Wcislo 1984, Danforth and Visscher 1993), or density independent (Trexler 1985, Rosenheim 1989). A more comprehensive understanding of density dependence in wild populations can help explain the evolution and continued persistence of aggregative nesting behavior (Rosenheim 1990) as well as the stability of host–parasitoid interactions (Hassell 1984). In this study, I investigated how variation in two key characteristics of solitary bee nest aggregations (cavity availability and progeny density) affects reproduction and brood parasitism rates in the blue orchard bee, Osmia lignaria Say (Hymenoptera: Megachilidae). This solitary bee species nests gregariously and appears to be attracted to aggregations with many actively nesting conspecifics (Tepedino and Torchio 1994, Bosch and Kemp 2001). Previous research in managed O. lignaria populations reported 36% higher overall brood cell production in 100-cavity nests than 400-cavity nests (Artz et al. 2013). Given this result, I expected to see a negative relationship between cavity availability and number of progeny produced in a wild O. lignaria population. Because the cleptoparasitic cuckoo bee S. montana appears to be visually attracted to nest sites with larger surface areas (Torchio 1989a) and nest sites with more cavities often have larger surface areas, I expected cavity availability would be positively correlated with S. montana brood parasitism rates. Finally, O. lignaria has been observed aggressively defending its nests against invading brood parasites, including S. montana (Torchio 1989a). Thus, I expected that the relationship between O. lignaria progeny density and brood parasitism rates would be inversely density dependent, potentially due to an increase in host vigilance and/or nest defense. Methods Study System The blue orchard bee (Osmia lignaria) is a solitary cavity-nesting species native to North America. After mating, a female selects a cavity and lays individual eggs provisioned with a mass of nectar and pollen and separated by mud partitions (Levin 1966). Females generally select hollow twigs or beetle burrows, but will accept paper tubes as artificial nesting habitat (Williams and Tepedino 2003). Eggs hatch several days after oviposition and larvae proceed through five instars before developing into adults in the early fall. Individuals overwinter in the natal nest as adults and emerge the following spring. The blue orchard bee is attacked by a diversity of parasites and parasitoids during nesting and development, sometimes resulting in high mortality rates prior to adult eclosion (Bosch and Kemp 2001). These parasites use a wide variety of strategies for gaining entrance to the host nest, some of which are highly dependent on host foraging behavior. The blister beetle Tricrania stansburyi (Coleoptera: Meloidae) is a phoretic cleptoparasite that latches on to foraging bees at flowers and is carried back to the host nest (Torchio and Bosch 1992). In contrast, the cuckoo bee Stelis montana enters the host nest to lay an egg while the female is foraging (Torchio 1989a). Because the two species use different strategies to locate and access the host nest, they may also exhibit different responses to changes in host density. Specifically, a parasite that actively locates host nests using visual and/or olfactory cues (S. montana) may be more likely to exhibit density dependence than a phoretic species that relies on passive transport to the host nest (T. stansburyi). Study Design In March 2015, I selected three regions of riparian habitat with naturally occurring O. lignaria populations in Kamas, Utah. The three sites were located within 8 km of each other and had similar plant species composition. I refer to the sites here as Big Pole (40°31′33.70″N 111°17′38.20″W), Provo River (40°34′23.61″N 111°13′6.60″W), and Silver Creek (40°34′53.96″N 111°14′30.48″W). In April 2015, I set up a total of 60 pine nesting structures with predrilled cavities (‘nest blocks’) across the three study locations. I deployed three nest block sizes at each study location: small (15 nest cavities; 10 × 10 × 16 cm), medium (49 cavities; 31 × 13 × 16 cm), and large (96 cavities; 50 × 15 × 16 cm). To allow for removal and examination of individual nests, I lined all cavities with paper nesting tubes (7.5 mm × 15 cm [diameter by length]). I also covered the back of each nest block with aluminum foil tape to prevent moisture from reaching the nest tubes. The number of nest blocks deployed at each site differed due to limitations in the number of trees. At Big Pole, the largest site, I set up 36 nest blocks along a 1,500 m transect. At Silver Creek and Provo River, I set up 18 and 6 nest blocks, respectively. Using baling wire, I attached all nest blocks 1 m aboveground on the S/SE side of narrowleaf cottonwood trees (Populus angustifolia) to maximize exposure to morning sunlight. When hanging nests, I selected trees separated by at least 5 m and haphazardly distributed the nests throughout each site to ensure that no two nest blocks of the same size occurred in close proximity. The nesting period for O. lignaria began in late April 2015 and concluded in mid-June 2015. I collected all nests in late June 2015 and incubated the paper nest tubes at room temperature (20–21°C) for 2 months to allow O. lignaria to mature to adulthood. During this period, I suspended blacklights over dishes of soapy water near the paper nest tubes to capture emerging multivoltine parasitoids (e.g., Monodontomerus sp., Torymidae) and prevent reparasitism of developing bees. In late August 2015, I used digital radiography (8-s exposure at 20 kVp) (Faxitron 43804N; Faxitron Bioptics, Tucson, AZ, USA) to record the abundance and species identity of parasitic species that develop inside the original host cocoon (Fig. 1). I then dissected each nest tube and recorded the weight and abundance of male and female O. lignaria progeny as well as the abundance of the congener Osmia californica Cresson (Hymenoptera: Megachilidae). The two Osmia species are easily distinguished based on cocoon morphology and mud partition composition (O. californica uses a mixture of masticated leaf and mud in nest partitions, whereas O. lignaria uses mud only) (Levin 1966). However, because both T. stansburyi and S. montana spin their own cocoons rather than developing inside the original host cocoon, I inferred the original host of parasitized cells based on the species identity of unparasitized cells within the same nest cavity. If all cells in the nest cavity were parasitized, I closely examined the mud wall architecture to determine whether it contained a mud–leaf mixture (O. californica) or mud only (O. lignaria). Fig. 1. View largeDownload slide Digital X-ray of O. lignaria paper nesting tubes, showing (a) adult T. stansburyi, (b) S. montana prepupa, and (c) adult female O. lignaria (credit: Shahla Farzan). Fig. 1. View largeDownload slide Digital X-ray of O. lignaria paper nesting tubes, showing (a) adult T. stansburyi, (b) S. montana prepupa, and (c) adult female O. lignaria (credit: Shahla Farzan). Analyses I used a series of generalized linear mixed models (GLMMs) and linear mixed models (LME) to analyze the effect of cavity availability and O. lignaria progeny density on measures of brood parasitism and bee reproduction (lme4 pkg, R Development Core Team 2017). In this study, cavity availability refers to the number of cavities per experimental nest block and progeny density to the number of progeny per available nest cavity. I included cavity availability as a fixed factor and site location as a random factor in all models. To compare nested models, I used chi-square tests of log-likelihood values. To check for normality, I used the Shapiro–Wilk test and visually assessed quantile–quantile plots. For post hoc pairwise comparison testing, I used Tukey’s honestly significant difference test (multcomp pkg, R Development Core Team 2017). Because the two most common cleptoparasites in the study region have different strategies for accessing host nests, I analyzed them separately in all parasite-related models. For the purposes of this study, parasitism rate is defined as the proportion of parasitized nest cells. To compare parasitism rates by nest cavity availability, I used a binomial GLMM with a logit link. I also investigated the correlation between parasitism rate and log-transformed bee progeny density using LME, with progeny density included as an additional fixed factor. Bee progeny density was log-transformed to normalize error variance. To examine the influence of cavity availability on the number of O. lignaria progeny produced, I used a Poisson GLMM with a log link. Although I deployed the same number of nests per nest block size (n = 20; see Study design), the number of nest blocks with at least one O. lignaria progeny varied (15-cavity: n = 14; 49-cavity: n = 19; 96-cavity: n = 20). I also analyzed the effect of cavity availability on O. lignaria progeny weight using LME. There was a significant sex by treatment interaction (SE = 0.003, t = −2.53, P = 0.01); therefore, I opted to analyze male and female weight separately. Results Brood Parasitism There was a negative effect of nest cavity availability on S. montana parasitism rates (χ2 (2) = 11.46, P < 0.01, Fig. 2a). On average, S. montana parasitism rates were higher in 49-cavity nest blocks (0.10) than in 96-cavity nests (0.07) (SE = 0.21, z = 3.36, P < 0.01). There was no significant effect of nest cavity availability on T. stansburyi parasitism rate (χ2 (2) = 0.92, P = 0.63, Fig. 2b). Fig. 2. View largeDownload slide Brood parasitism rates by nest block size for (a) S. montana and (b) T. stansburyi. Fig. 2. View largeDownload slide Brood parasitism rates by nest block size for (a) S. montana and (b) T. stansburyi. For nest blocks that had S. montana and/or T. stansburyi present, brood parasitism rate was negatively correlated with log-transformed O. lignaria progeny density. Specifically, log-transformed bee progeny density was negatively correlated with S. montana parasitism rate (χ2 (1) = 8.72, P < 0.01, Fig. 3a) and T. stansburyi parasitism rate (χ2 (1) = 7.76, P < 0.01, Fig. 3b). Fig. 3. View largeDownload slide Brood parasitism rates by O. lignaria progeny density for (a) S. montana and (b) T. stansburyi. Data shown are not transformed. Fig. 3. View largeDownload slide Brood parasitism rates by O. lignaria progeny density for (a) S. montana and (b) T. stansburyi. Data shown are not transformed. Bee Reproduction There was a strong positive effect of nest cavity availability on the total number of female (χ2 (2) = 217.54, P < 0.0001, Fig. 4a) and male O. lignaria progeny produced (χ2 (2) = 444.76, P < 0.0001, Fig. 4b). In contrast, nest cavity availability had variable effects on bee progeny weight. There was no significant difference in female O. lignaria weight across the three nest block sizes (χ2 (2) = 0.15, P = 0.93, Fig. 5a). However, males produced in 15-cavity nest blocks weighed significantly less than males in 49- or 96-cavity nests (χ2 (2) = 11.28, P < 0.01, Fig. 5b). On average, males from 96-cavity nests were 8% heavier than males in 15-cavity nests (SE = 0.001, z = −3.35, P < 0.01), while males in 49-cavity nests were 9% heavier than males in 15-cavity nests (SE = 0.002, z = –2.58, P < 0.05). Fig. 4. View largeDownload slide Number of (a) female and (b) male O. lignaria progeny produced per nest block across the three size classes. Fig. 4. View largeDownload slide Number of (a) female and (b) male O. lignaria progeny produced per nest block across the three size classes. Fig. 5. View largeDownload slide Weight of (a) female and (b) male O. lignaria progeny by cavity availability. Fig. 5. View largeDownload slide Weight of (a) female and (b) male O. lignaria progeny by cavity availability. Discussion In this study, specific features of O. lignaria nesting aggregations affected both brood parasitism rates and measures of bee reproduction. In particular, nest cavity availability had a negative effect on S. montana brood parasitism rates. Log-transformed O. lignaria progeny density was also negatively correlated with brood parasitism rate for S. montana and T. stansburyi. Finally, cavity availability had a significant positive effect on male O. lignaria body weight, with the highest progeny weights produced in nests with the most cavities. These results suggest that progeny density and cavity availability can be important factors affecting reproduction and progeny survival in this solitary bee species. Brood Parasitism Nest cavity availability negatively affected S. montana brood parasitism, with the lowest parasitism rates occurring in the largest nest block size (96-cavity, Fig. 2a). Because there were more O. lignaria progeny produced in 96-cavity than in 15-cavity nest blocks, this may have diluted parasitism risk. If S. montana females are limited by their oocyte maturation rate and/or by the handling time required to parasitize each host, this may have resulted in comparatively lower parasitism rates for nest blocks with more potential hosts. In other words, an S. montana female may have been able to sequentially parasitize more bee progeny in a 15-cavity nest than a larger nest block with more hosts. Because S. montana must oviposit in open (uncapped) brood cells (Torchio 1989a), a female waiting for oocytes to mature may miss opportunities to parasitize host nests. No published studies to date have examined oocyte maturation rates in S. montana. However, the congeners S. murina, S. ater, and S. elongativentris average between 2 and 2.67 mature oocytes per individual at any given point in time (Rozen and Hall 2011), suggesting Stelis spp. may be somewhat limited in the number of brood cells they can parasitize sequentially. Another possible explanation for comparatively higher parasitism rates in 15-cavity nest blocks is that searching S. montana females were attracted to nests with fewer cavities. However, this seems unlikely given previous observations of S. montana host searching behavior (Torchio 1989a). Female S. montana systematically inspect wood surfaces, returning to nests with larger surface areas more frequently and for longer periods of time than nests with smaller surface areas (Torchio 1989a). Brood parasitism in this system exhibited inverse density dependence (that is, declining rates of S. montana and T. stansburyi parasitism with increasing O. lignaria progeny density; Fig. 3). There are several possible factors that may explain reduced brood parasitism rates in dense nesting aggregations. As noted previously, S. montana females may be limited in the number of mature oocytes available, contributing to inversely density-dependent parasitism. Similarly, in meloid beetles, the time between successive ovipositions can range from 2.5 to 9.2 days, potentially due to limitations in oocyte maturation rate (Lückmann and Assmann 2006). Females nesting in denser aggregations may have also benefited from improved group vigilance and/or group defense, particularly with regard to the mobile cleptoparasitic species S. montana. Female O. lignaria and O. californica have been observed vigorously defending their own nests against S. montana (Torchio 1989a), although it is unclear whether they also defend nesting aggregations. In this study, there was a strong negative correlation between brood parasitism rate and log-transformed O. lignaria density (Fig. 3). However, these results should be interpreted cautiously. Studies of density dependence in parasitoids of other solitary hymenopterans have yielded mixed results across systems (Wcislo 1984, Rosenheim 1990, Danforth and Visscher 1993, Strohm et al. 2001). Moreover, the direction of density dependence in host–parasitoid relationships may vary by year (Steffan-Dewenter and Schiele 2008). Although I attempted to control for spatial variation by including several site locations, this experiment spanned a single season. Additional studies conducted during the course of several years would be necessary to account for potential interannual variation in the direction and strength of density dependence. Bee Progeny Nest cavity availability had a significant, positive effect on O. lignaria male and female offspring count, with the largest numbers of progeny produced in the largest nest block size (96-cavity) (Fig. 4). Initially, these results appear to be at odds with two related studies in commercial almond orchards, which reported a negative relationship between nest cavity availability and O. lignaria brood cell production (Artz et al. 2013, 2014). However, both studies compared O. lignaria reproduction in two nest block sizes (100- and 400-cavity) and reported higher brood cell production in 100-cavity nests. Taken together, these results suggest an intermediate nest block size (ca. 100 cavities) may result in the highest O. lignaria progeny production. Because I did not track individual female bees in this study, it is unclear whether comparatively higher progeny production in 96-cavity nests was due to higher numbers of nesting females, differences in per female reproductive output, or both. Thus, without individual-level data on nesting females, it is difficult to assess whether females preferred a certain nest block size. Nest cavity availability also significantly affected male O. lignaria progeny body weight. On average, males had the lowest weights in 15-cavity nests (0.06 g) as compared with 49- and 96-cavity nests (0.07 g) (Fig. 5b). Solitary bee body size is highly correlated with the weight of the pollen–nectar provision (Johnson 1988, Bosch and Vicens 2002). Pollen type can also affect O. lignaria progeny weight, with pollen from certain plant species apparently more suitable for larval growth and development (Levin and Haydak 1957). The effect of cavity availability on progeny weight may, therefore, be mediated by differences in female O. lignaria foraging behavior. First, if nests with fewer cavities are inherently less attractive to female bees than nests with more cavities, smaller and/or less competitive females may be compelled to nest there. These females may be more likely to underprovision their nests, producing smaller offspring. Alternatively, variation in O. lignaria emergence timing may drive differences in male progeny body weight across nest block sizes. For instance, if early emerging female O. lignaria prefer nests with more cavities, later emerging females will be more likely to occupy small nest blocks. As floral resource availability dwindles, these ‘late females’ may have to fly farther to provision their nests. Torchio and Tepedino (1980) reported that male progeny of late emerging O. lignaria weighed 20% less than those of early emerging bees and attributed this difference to a reduction in the quality and quantity of floral resources. Given that male brood cells are typically provisioned last (Torchio 1989b), declining floral resource availability could have a disproportionate effect on pollen–nectar provision weight in male cells. Finally, because 15-cavity nest blocks were physically smaller than 49- or 96-cavity nest blocks, it is possible that their occupants were less buffered against changes in ambient temperature. Nest microclimate can have dramatic effects on the development and survival of cavity-nesting hymenopterans (Frankie et al. 1988). In a recent study, Osmia bicornis (Linnaeus) (Hymenoptera: Megachilidae) larvae exposed to various temperature treatments during development showed significant differences in adult weight (Radmacher and Strohm 2010). At higher temperatures, larvae consumed less pollen and gained less weight per unit of provisions, resulting in significantly reduced adult weights (Radmacher and Strohm 2010). Although it is possible that smaller nest blocks reached higher internal temperatures, which in turn negatively affected male O. lignaria weight, it seems unlikely given that there was no significant difference in female progeny weight across the three nest block sizes (Fig. 5a). Conclusions The results of this study suggest that nest cavity availability and progeny density can significantly affect brood parasitism and reproduction in the blue orchard bee. Brood parasitism in this system was inversely density-dependent, with comparatively lower parasitism rates at high host densities. Nest cavity availability not only negatively affected S. montana brood parasitism rates but also had a positive effect on both the total number of progeny produced and male progeny body weight. Within nest aggregations, there are likely multiple selective forces operating concurrently that vary across space and time. Additional studies that attempt to identify these selective pressures will help to refine our understanding of the evolution of aggregated nesting in solitary hymenopterans. Acknowledgments I would like to thank L.H. Yang for helpful feedback that improved this research study, K.A. Johnson for fieldwork assistance, M.J. Allan for study site usage, T.L. Pitts-Singer for the use of bee nesting materials, G.I. Wardell for providing assistance with specimen X-rays, R.W. Thorp for specimen identification, and J.A. Rosenheim, N.W. 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Environmental Entomology – Oxford University Press
Published: Feb 1, 2018
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