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Prairie restorations and bees: The potential ability of seed mixes to foster native bee communities
Basic and Applied Ecology 16 (2015) 64–72
Prairie restorations and bees: The potential ability of seed mixes to foster native bee communities Alexandra N. Harmon-Threatta,∗ , Stephen D. Hendrixb a b
Department of Entomology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA Department of Biology, Washington University in St. Louis, St. Louis, MO 63130, USA
Received 7 March 2013; accepted 9 November 2014 Available online 15 November 2014
Abstract Restoring native habitat is considered critical to conserving native pollinators threatened by habitat loss and degradation, but little is known about whether ecological restorations, most of which do not target pollinators, can predictably support pollinator communities. In this study we compare plant species richness in common commercial prairie seed mixes to remnant prairies, and we take a modeling approach to examine the ability of these seed mixes to attract bee communities relative to native prairie remnants. Using a large data set from native prairies in Iowa consisting of 70 bee species (≈2700 bee specimens) associated with 54 native prairie plants, we constructed species accumulation curves to model the number of bee species potentially attracted to a restoration with the addition of each plant in a seed mix. Our modeling results indicate commercial prairie mixes will accumulate species at rates similar to prairie remnants, but the bee species richness will be lower than remnants because the plant species richness in samples from prairie remnants is twice that of the average commercial seed mix. However, when commercially available seed mixes were modeled to always include four plant species that were exceptionally attractive to native bee species, most mixes attracted significantly more bees than predicted if random species were added. This further suggests that seed mixes and the resulting restorations do not adequately provide for pollinators and could be significantly improved with the addition of a small number of species. Although the particular optimal species additions to seed mixes will vary regionally, adding species functionally equivalent to those we identify may significantly improve restoration of ecological services provided by native bees.
Zusammenfassung Die Wiederherstellung von natürlichen Lebensräumen ist entscheidend für den Schutz einheimischer Bestäuber, die durch Habitatverlust und -degeneration bedroht sind, aber wenig ist darüber bekannt, ob ökologische Renaturierungen, die meist nicht auf die Bestäubergemeinschaften abzielen, diese vorhersagbar fördern können. In dieser Untersuchung vergleichen wir den Artenreichtum der Pflanzen in üblichen Samenmischungen zur Prärierenaturierung, und wir wählten einen Modellierungsansatz, um die Attraktivität dieser Samenmischungen für Bestäuber im Vergleich zu natürlichen Präriefragmenten abzuschätzen. Wir nutzten einen großen Datensatz bestehend aus 70 Bienenarten (∼2700 Individuen) und 54 einheimischen Präriepflanzen in natürlichen Prärien in Iowa und konstruierten Artenakkumulationskurven, um die Zahl der Bienenarten zu bestimmen, die potentiell bei einer Renaturierung durch eine zusätzliche Pflanzenart in einer Saatmischung hinzugewonnen werden könnte. Unsere Modellierungsergebnisse zeigen, dass kommerzielle Präriemischungen Arten in ähnlicher Weise akkumulieren wie
∗ Corresponding
author. Tel.: +1 217 333 3108, fax: +1 217 2443499. E-mail address: [email protected] (A.N. Harmon-Threatt).
http://dx.doi.org/10.1016/j.baae.2014.11.001 ¨ 1439-1791/© 2014 Gesellschaft f¨ur Okologie. Published by Elsevier GmbH. All rights reserved.
A.N. Harmon-Threatt, S.D. Hendrix / Basic and Applied Ecology 16 (2015) 64–72
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natürliche Präriefragmente. Dabei wird aber der Artenreichtum der Bienen geringer als in den Präriefragmenten sein, weil hier der Artenreichtum doppelt so hoch ist wie in kommerziellen Samenmischungen. Wenn indessen kommerziell angebotene Samenmischungen im Modell so verändert wurden, dass sie immer vier für Bienen außergewöhnlich attraktive Pflanzenarten enthielten, zogen die meisten Mischungen signifikant mehr Bienenarten an als bei Hinzufügung zufälliger Arten zu erwarten gewesen wäre. Dies legt desweiteren nahe, dass Samenmischungen und die resultierenden Renaturierungen Bestäuber nicht adäquat versorgen und durch die Zugabe von einigen wenigen Samenarten signifikant verbessert werden könnten. Wenn auch im Einzelnen die optimalen Ergänzungen regional variieren können, könnte die Ergänzung mit Pflanzenarten, die funktionell denen, die wir identifizierten, entsprechen, die Wiederherstellung von Ökosystemdiensten, die von einheimischen Bienen geleistet werden, signifikant verbessern. ¨ © 2014 Gesellschaft f¨ur Okologie. Published by Elsevier GmbH. All rights reserved.
Keywords: Pollinator; Bee richness; Bee conservation; Prairie; Iowa; Native plants; Grasslands.
Introduction Ecological restoration of declining and degraded habitats is typically designed for relatively few plant and animal species of concern and has historically focused on recreating botanical compositions and structural features of the non-degraded habitat (Young 2000; Ruiz-Jaen & Aide 2005). More recently, as the field of restoration ecology integrates with the science of conservation biology, restoration of functional aspects of ecosystems and their impact on sustainability of ecosystem services are now receiving equal attention (Devoto, Bailey, Craze, & Memmott 2012; Montoya, Rogers, & Memmott 2012). In practice, however, while restoration of topography, soil and plant diversity as well as phylogenetic diversity promote diversity of some non-target species such as arthropods (Dinnage, Cadotte, Haddad, Crutzinger, & Tilman 2012), in about two-thirds of examined restorations there is little or no data supporting the assumption that higher trophic levels and non-target species will colonize afterwards (Ruiz-Jaen & Aide 2005). Because the colonization of these restorations by such species is dependent on their dispersal to the site and on the availability of all needed resources, the actual impact of restored lands in promoting diversity and sustaining ecosystem functions is likely to be highly variable. In this study, we used known associations of prairie plants and insects to predict how seed mixes of varying plant richness might restore species richness of an important group, pollinators. Seed mixes used to restore land offer an effective way to introduce a diversity of plants to new and existing restorations, but can vary significantly in the species richness of forbs which could, in turn, impact their ability to support and attract higher trophic levels. Seed inclusion in mixes, however, is frequently driven by practical and economic considerations such as germination success, availability, or market demand, often without regard for their ecological role in restorations. Furthermore, restoration projects can have a number of immediate goals other than maximizing diversity across trophic levels, including suppressing invasive species (Skinner, van der Grinten, & Gover 2012), promoting diversity indirectly (Fiedler, Landis, & Arduser 2011) and increasing floral
diversity for the benefit of specific wildlife such as game birds (Draycott 2012), songbirds (Ortega-Álvarez & LindigCisneros, 2012) and butterflies (Shepherd & Debinski, 2005). Here we investigate whether plant species richness in seed mixes is similar to richness in remnant prairies and we model the ability of seed mixes to attract and support bee communities relative to native prairie remnants. Pollinators are one non-target functional group that can benefit from restored habitat (Winfree 2010) and some evidence has shown that restoration can increase pollinator diversity and abundance (Fiedler et al. 2011; Williams 2011). Restorations that improve pollinator diversity are increasingly important in promoting the success and stability of ecosystems (Winfree, Williams, Gaines, Ascher, Kremen 2008; Potts, Biesmeijer, Kremen, Neumann, Schweiger et al. 2010; Garibaldi, Steffan-Dewenter, Winfree, Aizen, & Bommarco et al. 2013) because of declines in bumble bees (Cameron, Lozier, Stange, Koch, Cordes et al. 2011) and other native bees (Burkle, Marlin, & Knight 2013) (but see Bartomeus, Ascher, Gibbs, Danforth, Wagner et al. 2013). Reciprocally, pollinator diversity can help support the success of prairie restorations by providing pollination services to native flowering forbs (Slagle & Hendrix 2009) and to important agricultural products (Winfree et al. 2008). Thus, pollinators that visit and use restored sites will be important to long-term maintenance of plant diversity and community structure. Using remnant tallgrass prairies to empirically measure the association of specific pollinators with particular plant species, we model how plant species included in seed mixes for prairie restoration might help restore pollinator communities. We focus on bee species because they are the dominant pollinators in most ecosystems (O’Toole & Raw, 1991), including the tall grass prairie biome in the central USA, but little work has been done to evaluate and improve mixes specifically for bees (Winfree 2010). First, we characterize the plant species richness of seed mixes compared to remnant prairies and then using models of bee species accumulation, we address two questions about seed mixes: 1) Are plant communities created using seed mixes expected
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to have similar bee richness as remnant prairies? 2) Can we increase the bee richness in plant communities created using seed mixes by selectively adding a few plant species that are visited by more bees in remnant prairies than expected given their abundance regionally or at a site? We hypothesize that seed mixes will not provide adequate resources to attract a richness of bee species equivalent to native prairie remnants because the mixes contain fewer plant species, but that the addition of a few plant species to these mixes will improve their attractiveness to bees.
collection was unrelated to either abundance or species richness of bees collected (all r values, <0.17, all p values, >0.75). At all sites plant abundance and diversity were quantified by directly counting the number of ramets of each forb species in flower in 5 m by 100 m strip plots within the 1 ha plots established for bee sampling. The number of flowering ramets is a reasonably accurate proxy for floral resources on prairies when sampling over large areas at many sites (Hines & Hendrix 2005) because the dominant families on prairies (Apiaceae, Asteraceae and Fabaceae) (see Results) have similar inflorescences with many flowers, a few of which open daily over a number of days. Plant surveys were conducted within ±3 days of each bee sampling at all sites. Flowering forb species were identified using local and regional guides (McGregor, Barkley, Brooks & Schofield 1986; Christiansen & Müller 1999). The original bee data set consisted of 2934 records of 82 bee species on 71 plant species. This was reduced to 2731 records of 70 bee species collected from 54 plants (Appendix A: Table 1) after invasive plants and their associated bees, cleptoparasitic bees and plant species for which no seeds were commercially available were removed. The 12 cleptoparasitic species (42 individuals; about 1.4% of total) were removed prior to analysis because their presence is dependent on not only flower diversity but also specific host species abundance and thus cannot be reliably modeled in this context. When a bee was caught on a plant that was not present in the plant survey an abundance of 1 was assigned to that plant species at that site (see Appendix A: Table 3). This added on average only two plant species and one bee species at each site.
Materials and methods Remnant prairie sampling From 2002 to 2004 we sampled monthly from May through August seven remnant prairies in the northwest one-quarter of Iowa, ranging in size from 10 to 80 ha (Table 1). The bee community was sampled by hand-netting from flowers and inflorescences in two to three 1-ha plots within each site. Sampling was conducted for 1 h in the morning (9 am to 12:30 pm) and again for 1 h in the afternoon (12:30 to 4 pm) because different bee species are active at different times of day (Stephen, Bohart, & Torchio 1969). We divided plots in half along their east-west axes, and the two collectors simultaneously sampled opposite 0.5 ha sides for 15 min, and then switched sides for 15 additional minutes for a total of 1 h sampling. Sampling time was based only upon search time and did not include the time required to handle bees after netting. The flowering species being used by a bee was noted at the time of capture. We conducted bee sampling only in temperatures greater than 15.5 ◦ C. Winds on prairies are highly variable over time and in local space (e.g. within a plot) because of topographical relief. Wind speeds during collecting were generally between 0 and 15 km/h; if winds were greater than 20 km/h collecting was temporarily suspended until wind gusts abated and bees reappeared. Adverse weather conditions prevented sampling at one prairie in August one year and the number of plots sampled differed between years at some sites because of flooding. As a result, sampling varied between sites from a total of 22–26 h. The number of hours of
Database of seed mixes In spring 2012, we identified four seed companies or organizations specializing in local seed for Iowa prairie restorations (Appendix A: Table 2). From each of these suppliers we selected seed mixes designed for prairies of varying types and species richness, or for the Conservation Reserve Program administered by the US Department of Agriculture Farm Service Agency, and we made an effort to cover the spectrum of mix types and diversities available from each. In
Table 1. Summary of site information and statistics of the bee and native plant species community from hand-netting samples at seven Iowa state prairie preserves. Bee abundance and richness values do not include cleptoparasitic species or bees associated with non-native plants. Prairie preserve
County
Size (ha)
Hand-netting sampling (h)
Bee abundance
Bee species richness
Plant species richness
Prairie type*
Anderson Cayler Doolittle Kalsow Kirchner Mori Steele
Emmet Dickinson Story Pocahontas Clay Clay Cherokee
81 65 10 65 65 16 81
26 26 22 26 23 24 24
266 535 501 595 284 260 288
31 39 31 39 38 32 32
39 35 33 34 37 26 34
1 1 2 2 3 1 1
*1 = Mesic prairie; 2 = Pothole prairie complex with seasonal marshes; 3 = Pothole prairie complex with year-round wetlands.
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total we examined 42 seed mixes containing between 4 and 60 species of forbs and a number of grasses. To ensure proper comparison between mixes and remnant prairies, we removed both rare plant species included in mixes but not found in remnant prairies and plant species that bloomed outside of the bee sampling periods. Inclusion of these plant species could unjustifiably underestimate how attractive to pollinators a seed mix would be relative to a remnant prairie. Also, we combined closely related species in mixes that were similar in bloom time and flower characteristics related to pollination (e.g. Aster spp.), typically at the genus level, and we similarly combined these in the empirical data if they were not previously combined because of potential misidentifications in the field (see Appendix A: Table 1). Less than 20% of the database was reduced by grouping species in this manner. Species in the Asteraceae family were most commonly combined because of its high diversity. We do not expect data manipulations to adversely affect our analysis because many of the species that were combined are locally abundant in the specific areas near the four commercial seed suppliers but rare across the greater prairie ecoregion.
Identifying bee plants Bee visitation to plant species is dependent on a number of factors including local plant species abundance, which can affect attractiveness of bees to species, and geographic distribution, which can affect the pool of bees potentially attracted to a plant. Thus, to identify plants in our samples that might be particularly attractive to bee species across many remnant prairies (herein referred to as “bee plants”), we first analyzed the effect of total site abundance, distribution across sites and regional distribution of each plant species on bee richness. Total site abundance was defined as the total number of flowering ramets of a species across all sites and distribution across sites was defined as the total number of sites (out of seven) at which a species occurred. Regional distribution was determined using dot distribution maps and was defined as the total number of counties (out of a possible 1039) in the Great Plains region in which a plant species had been collected (McGregor & Barkley 1977). This analysis focused on the 30 plants identified to species visited by at least three bee species (Appendix A: Table 1) because plants visited by fewer bee species were unlikely to qualify as bee plants. Preliminary analyses using Pearson product-moment correlations to test for relationships between these three predictor variables of abundance showed that the number of sites at which a plant was recorded in our surveys was significantly related to total site abundance of flowering ramets (r = 0.771, p = 0.001) and regional distribution (r = 0.398, p = 0.033), so we dropped number of sites occupied from further analyses. Additionally, number of sites occupied has a small range (1–7) for the more than 50 plants in the analysis compared to over 40 values when the variable total site abundance is used
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which increases the power of the analysis. Total site abundance and regional distribution were not related (r = −0.071, p = 0.678). We used least-square regression analysis to examine the relationship between regional distribution and bee species richness (adjusted R2 = 0.196, p = 0.008) from which we extracted residuals which were then regressed against the total abundance of ramets across all sites. In this latter analysis all plant species outside the upper 95% confidence level were categorized as “candidate bee plants”. To determine if candidate bee plants were more consistently attractive than expected across different sites, we inspected the least-square regression between local plant abundance at a site and number of bees associated with that plant at the site. Candidate bee plants were then elevated to the status of bee plants if 50% or more of the sites for a plant species fell outside the 95% confidence limit.
Model Species accumulation curves model how species richness or diversity changes as sample size increases. These models randomly draw plant species and record how many new bee species are added with the addition of each plant. This is then permutated a number of times to produce a mean species accumulation curve. First, we modeled the accumulation of bee species in each of the seven remnant prairies. Next we modeled the potential accumulation of bee species in each of the 42 mixes. To account for the natural variability in plant species, plant abundance and bee species between prairie remnants, the model selects the plant species in each mix first and then selects a sample from any of the seven prairie remnants that contained that plant. The process continues until all plant species in a mix are chosen and then permutated 1000 times to produce a mean curve of bee accumulation for a given mix. To limit an artificially high accumulation of rare species when selecting across sites, a reduced data set restricted to the 52 bee species occurring in more than one site was used to model the potential accumulation of bees with mixes. To determine how the seed mixes accumulate bee species compared to remnant prairies, we created a mean species accumulation curve and confidence interval using the same procedure for the mixes with the plant species observed in a single prairie chosen from across all prairies. The accumulation for each mix is then overlaid on the 95% confidence interval of all the remnant prairies to determine whether the expected mean bee accumulation for mixes fell within the range of remnant prairies. To determine whether mixes could be amended to improve their suitability for bees, we modeled the accumulation of bees when seed mixes always included the four plant species from our data shown to qualify as bee plants (see Results). We compared the accumulation of bees for seed mixes that were amended with bee plants to the mixes amended with the same number of randomly drawn plant species which
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Table 2. Count and relative abundance of the ten most abundant plant and bee species in hand-netted samples. A) Plant species
Fig. 1. The accumulation of bee species with increasing number of plant species in each of seven prairie remnant preserves sampled in northwest Iowa. Open points indicate type 1 prairies, closed points type 2 and asterisks type 3 (see Table 1).
were added to ensure that mixes maintained the same plant richness as those amended with bee plants. As in previous analyses, a plant was chosen from a random prairie and used to construct bee associations for plants found in each mix; the process was repeated 1000 times to produce a mean species accumulation curve and associated 95% confidence interval envelope. We used a Wilcoxon paired sign test to compare bee species accumulated between the two types of species additions. We used a multiple response permutation procedure (MRPP)–a permutation method that is similar to MANOVA but considered more robust for ecological data–to determine if bee–plant interactions were significantly different between prairies. MRPP uses a distance matrix to compare the similarity within and between groups and determine whether there is significant difference in the interactions observed (McCune and Grace 2002). All analyses were conducted in R v 2.15.1, using the vegan package for MRPP and scripts written by the first author.
Results Samples from remnant prairies contained between 26 and 39 native flowering plant species and between 31 and 39 bee species (Table 1, Fig. 1). Bees were collected on about 60% of the flowering forb species identified in the plant surveys with the other 40% not having any observed visitors. Plant species on which bees were collected by hand-netting were visited by 0-18 bee species at any individual prairie. The 10 most abundant plant species overall in the plant surveys accounted for about 72% of all flowering forb ramets and were dominated by members of the Asteraceae (Table 2). Even though abundances of plants were highly variable between remnants (Appendix A: Table 3), bee–plant associations between remnant prairies did not differ significantly (MRPP, A = 0.003,
Plant species (family)
Number of ramets (% of total)
Zizia aurea (Apiaceae) Pycnanthemum virginianum (Lamiaceae) Anenome canadensis (Ranunculaceae) Ratibida pinnata (Asteraceae) Coreopsis palmata (Asteraceae) Heliopsis helianthoides (Asteraceae) Lathyrus venosa (Fabaceae) Achillea millifolium (Asteraceae) Monarda spp. (Lamiaceae) Dalea purpurea (Fabaceae)
4013 (16.5) 3447 (14.2) 3203 (13.2) 1679 (6.9) 1355 (5.6) 1351 (5.2) 1027 (4.2) 870 (3.6) 836 (3.4) 742 (3.1)
B) Bee species Bee species (family)
Number of bees (% of total)
Melissodes trinodis (Apidae) Bombus griseocollis (Apidae) Andrena ziziae (Andrenidae) Svastra obliqua (Anthophoridae) Halictus ligatus (Halicitidae) Andrena illinoiensis (Andrenidae) Andrena quintilis (Andrenidae) Hylaeus affinis (Colletidae) Augochlorella aurata (Halictidae) Andrena helianthiformis (Andrenidae)
478 (17.3) 309 (11.2) 199 (7.12) 189 (6.8) 188 (6.8) 160 (5.8) 134 (4.8) 99 (3.6) 96 (3.5) 90 (3.3)
p = 0.120). The 10 most common bee species account for 71% of all individuals and were dominated by members of the Andrenidae and Apidae (Table 2). Seed mixes contained an average of 17.6 plant species, approximately half as many as the average for prairies. When reduced to just the plant species observed in remnant prairies, the average was 14.9 species with a range of 4–28. After reducing modeling results to simulations that occurred at least 5% of the time, mixes with up to 20 plant species accumulated between 6.6 and 31.8 bee species which fell within the confidence intervals for the model of bee species accumulation on the remnant prairies (Fig. 2). We identified eight species in remnant samples as candidate bee plants (see Appendix A: Fig. 1). These were Amorpha canescens (Fabaceae), Cicuta maculata (Apiaceae), Coreopsis palmata (Asteraceae), Dalea purpurea (Fabaceae), Heliopsis helianthoides (Asteraceae), Ratibida pinnata (Asteraceae), Solidago rigida (Asteraceae) and Zizia aurea (Apiaceae). Four of these species were classified as bee plants because the bee richness associated with each plant species fell above the upper 95% confidence limit of the regression between bee richness and log-transformed plant abundance in at least half of the sites at which they occurred.
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Fig. 2. The mean accumulation of bee species for the remnant prairies (heavy black line), and the mean accumulation of bees for each of 42 commercial seed mixes (gray lines) across 1000 simulations reduced to plant richness levels occurring in more than 5% of the simulations. Confidence intervals are for the mean across remnant prairies.
Bee plants were A. canescens (5 of 7 sites), D. purpurea (4 of 7 sites), R. pinnata (4 of 7 sites) and Z. aurea (5 of 7 sites). The remaining four species failed the criterion (C. palmata [2 of 6 sites], C. maculata [1 of 4 sites], H. helianthoides [2 of 7 sites] and S. rigida [1 of 6 sites]). The number of candidate bee plant-site combinations outside the 95% CI at different prairies did not differ from random (χ = 2.70, d.f. = 6, p > 0.5). Three of the four bee plant species are among the top 10 most abundant plant species across all prairies (Table 2), but differed widely in abundance between prairies (see Appendix A: Table 3). Seed mixes contained on average only 2.1 of the four bee plants with 24 of the 42 mixes having two or fewer bee plants and only five mixes with all four bee plants. When seed mixes were modeled to ensure they included all four bee plants, the range of bee species accumulated by mixes was 23–31 bee species. Overall, models with amended mixes had significantly more bee species than mixes that were amended with random species (see Fig. 3, mean range (−0.01–11.8), z = 5.64, p = 0.000). Over 60% of the 37 mixes amended with bee plants accumulated five or more bee species than mixes amended with random plants (Fig. 3). Generally, mixes amended with bee plants had smaller confidence intervals in their total bee species richness than mixes amended with random species, indicating that even low-diversity mixes could benefit pollinators with the addition of a few plant species.
Discussion Our results indicate that the restoration of prairie plant diversity using commercially available seed mixes is likely to
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Fig. 3. The change in the mean bee richness for mixes amended with bee plants relative to mixes amended with random plants. Forb mixes were plotted in ascending order of plant richness (mix 1 = 5 species, mix 42 = 28 species). The dotted line indicates no difference between adding random plants or bee plants and the five mixes that contained all four bee plants are indicated on the zero line. Note: Order of mixes is different than Appendix A: Table 2.
benefit native bees (Fig. 2), a non-target group of organisms. Although mixes accumulated fewer total bee species than remnant prairies because they contain less than half of the forb richness (∼48%) (Fig. 2), all of the mixes fall within the confidence interval for bee species accumulations by remnant prairies. Given that relatively few mixes contain the typical richness of plant species of even the poorest native prairie remnant (26–39 species/0.05 ha) (Appendix A: Table 3), it is unlikely that most mixes can support a bee community as rich as a prairie remnant unless more plants are included. Our modeling analysis of amending mixes to increase attractiveness to bee communities indicates that the addition of a relatively few plant species can significantly increase the value of a restoration to a potential bee community. The four species we identified as particularly important (Amorpha canescens, Dalea purpurea, Ratibida pinnata and Zizia aurea) are potential keystone plants for bee communities in many parts of the tall grass prairie ecoregion because they are widely distributed–as revealed in the regional distribution analysis and the number of sites occupied–and are often abundant on prairies (Appendix A: Table 3). It is possible that their wide distribution and high local abundance may contribute to their selection as bee plants and this wide distribution of the bee plants may also imply that they are suitable for many locations throughout the tallgrass prairie region and could be widely used to restorations for bees. Further, as a group these bee plants flower across the blooming season from May (Z. aurea) to September (R. pinnata) and some are known to provide a rich source of pollen because of high flower number in inflorescences and high pollen/ovule ratios (A. canescens and R. pinnata) (Cruden & Miller-Ward 1981) thus making them highly beneficial to bee pollinators. All of these factors indicate that addition of a few plant species will improve bee community richness in restorations. If bee conservation is a direct or indirect goal of the prairie restoration, inclusion of a few key plant species to
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mixes is a cost-effective method to reach that goal when mixes have a relatively low number of plant species (Fig. 3). It is interesting to note that the five mixes that contain all four bee plants were not targeted for pollinators specifically and were devised by the seed companies rather than for the Conservation Reserve Program. Additionally, many of the plant species in “pollinator” mixes are much better suited for butterflies. This suggests much of the habitat that is set aside in various programs could be more beneficial to bees with only a few plant species added at a relatively low cost. It is worth noting that our estimates of bee richness based on hand-netting are likely an underestimation because 38% of the bee species in our remnant sample (27 of 70) are rare (only 1 or 2 individuals) (Appendix A: Table 1), a phenomenon not uncommon in bee diversity studies (Williams, Minckley, Silveira 2001; Potts, Vulliamy, Dafni, Ne’eman, & Willmer, 2003), indicating there are likely many more species at most remnants that were not collected. In addition, the use of pan trap sampling reveals numerous species not caught by hand-netting (Stephen & Rao 2007). Furthermore, some plant species in mixes likely serve as pollen and nectar sources for bee species, but were not represented in our remnants and thus we cannot estimate their contribution to restored prairies. One major assumption of our model is that plants included in mixes will establish and attract bee species in restored sites as they do in native remnants. Plant establishment in restored areas, however, is known to be highly variable (Carter & Blair 2012) and dependent on a myriad of site-specific features of the restored land such as methods used to clear and maintain it (i.e. tilling, burning or herbicides) (Campbell, Hanula, & Waldrop, 2007; Williams, Crone, Roulston, Minckley, Packer, et al., 2010) and land use history (Xu, Wan, Ren, Han & Jiang 2012). Similarly, bee attraction to prairie plant species is density dependent (see Methods: Identifying bee plants) and within our remnant prairies, abundances of species below 200 flowering ramets/ha attracted relatively few bee species. Bee attraction and persistence in a site is a community level phenomenon, not on an individual species level one, as the model treats it. Each bee species may require a particular group of plant species to persist in an environment, a factor we do not attempt to incorporate in the present model. Thus, we might expect highly variable responses in bee abundance, richness and composition in restored sites, particularly small ones. Although our model broadly takes into account the natural variation in plant abundance and attractiveness to bees by sampling across multiple prairies, we note three additional site characteristics (of many) that can affect bee communities in restored sites, but are not included in our model. First, the composition of the assembled bee community in restored areas will be partially dependent on the quality of the surrounding landscape (Hines & Hendrix 2005). Such landscape effects likely explain some of the variation in the rate
of species accumulations seen at prairie remnant preserves (Fig. 1) and the failure of bee plants in our study to attract more bee species than expected at some sites even when relatively abundant. Second, nesting availability is important to support a diverse bee community (Winfree, 2010), but cannot be included in the model because of unknown variation between restorations in their ability to support bee nesting. For example, absence of cavity-nesting bees may indicate a negative effect of fire on the standing dead stems they typically inhabit (Davis et al. 2008) and the presence of cleptoparasitic species (removed in our study) may indicate a healthy bee community (Sheffield, Pinder, Packer, Kevan 2013). Lastly, the size of restorations is not included in our model, but studies of small natural remnants indicate that they may attract and support bee communities as diverse as larger prairies, if their plant community is relatively rich (Davis et al. 2008; Hendrix, Kwaiser, Heard 2010). We would expect these factors to have a significant effect on the potential pool of bee species attracted to the plant species in restorations. While our study provides insights into possible overall species richness of bee communities in restorations, we recognize that empirically determining actual species composition of restorations will reveal additional important details about the effectiveness and management of restorations for bees. This modeling study is meant to provide preliminary insight into whether landscapes restored using standard mixes will be attractive to bee species. Monitoring of restored prairies will be needed to understand better how well the seed mixes being used actually attract pollinators, although our results suggest previously installed restorations and those using these standard mixes or similar ones are benefitting pollinator conservation, if not duplicating bee communities at prairie remnant sites.
Acknowledgments The authors would like to thank K. Kwaiser and K. Gaddis, for field assistance collecting bees and Kristen Chin for helping create the database of mixes. We thank the Center for Global and Regional Environmental Research, Iowa Living Roadway Trust Fund, Iowa Science Foundation, Prairie Biotic Research, and the Department of Biology for funding to SDH. Additional thanks are due to the Iowa Lakeside Laboratory and to the NSF-Postdoctoral Fellowship in Biology for funding to AHT while working on this project.
Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10. 1016/j.baae.2014.11.001.
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Available online at www.sciencedirect.com
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Prairie restorations and bees: The potential ability of seed mixes to foster native bee communities Alexandra N. Harmon-Threatta,∗ , Stephen D. Hendrixb a b
Department of Entomology, University of Illinois Urbana-Champaign, Urbana, IL 61801, USA Department of Biology, Washington University in St. Louis, St. Louis, MO 63130, USA
Received 7 March 2013; accepted 9 November 2014 Available online 15 November 2014
Abstract Restoring native habitat is considered critical to conserving native pollinators threatened by habitat loss and degradation, but little is known about whether ecological restorations, most of which do not target pollinators, can predictably support pollinator communities. In this study we compare plant species richness in common commercial prairie seed mixes to remnant prairies, and we take a modeling approach to examine the ability of these seed mixes to attract bee communities relative to native prairie remnants. Using a large data set from native prairies in Iowa consisting of 70 bee species (≈2700 bee specimens) associated with 54 native prairie plants, we constructed species accumulation curves to model the number of bee species potentially attracted to a restoration with the addition of each plant in a seed mix. Our modeling results indicate commercial prairie mixes will accumulate species at rates similar to prairie remnants, but the bee species richness will be lower than remnants because the plant species richness in samples from prairie remnants is twice that of the average commercial seed mix. However, when commercially available seed mixes were modeled to always include four plant species that were exceptionally attractive to native bee species, most mixes attracted significantly more bees than predicted if random species were added. This further suggests that seed mixes and the resulting restorations do not adequately provide for pollinators and could be significantly improved with the addition of a small number of species. Although the particular optimal species additions to seed mixes will vary regionally, adding species functionally equivalent to those we identify may significantly improve restoration of ecological services provided by native bees.
Zusammenfassung Die Wiederherstellung von natürlichen Lebensräumen ist entscheidend für den Schutz einheimischer Bestäuber, die durch Habitatverlust und -degeneration bedroht sind, aber wenig ist darüber bekannt, ob ökologische Renaturierungen, die meist nicht auf die Bestäubergemeinschaften abzielen, diese vorhersagbar fördern können. In dieser Untersuchung vergleichen wir den Artenreichtum der Pflanzen in üblichen Samenmischungen zur Prärierenaturierung, und wir wählten einen Modellierungsansatz, um die Attraktivität dieser Samenmischungen für Bestäuber im Vergleich zu natürlichen Präriefragmenten abzuschätzen. Wir nutzten einen großen Datensatz bestehend aus 70 Bienenarten (∼2700 Individuen) und 54 einheimischen Präriepflanzen in natürlichen Prärien in Iowa und konstruierten Artenakkumulationskurven, um die Zahl der Bienenarten zu bestimmen, die potentiell bei einer Renaturierung durch eine zusätzliche Pflanzenart in einer Saatmischung hinzugewonnen werden könnte. Unsere Modellierungsergebnisse zeigen, dass kommerzielle Präriemischungen Arten in ähnlicher Weise akkumulieren wie
∗ Corresponding
author. Tel.: +1 217 333 3108, fax: +1 217 2443499. E-mail address: [email protected] (A.N. Harmon-Threatt).
http://dx.doi.org/10.1016/j.baae.2014.11.001 ¨ 1439-1791/© 2014 Gesellschaft f¨ur Okologie. Published by Elsevier GmbH. All rights reserved.
A.N. Harmon-Threatt, S.D. Hendrix / Basic and Applied Ecology 16 (2015) 64–72
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natürliche Präriefragmente. Dabei wird aber der Artenreichtum der Bienen geringer als in den Präriefragmenten sein, weil hier der Artenreichtum doppelt so hoch ist wie in kommerziellen Samenmischungen. Wenn indessen kommerziell angebotene Samenmischungen im Modell so verändert wurden, dass sie immer vier für Bienen außergewöhnlich attraktive Pflanzenarten enthielten, zogen die meisten Mischungen signifikant mehr Bienenarten an als bei Hinzufügung zufälliger Arten zu erwarten gewesen wäre. Dies legt desweiteren nahe, dass Samenmischungen und die resultierenden Renaturierungen Bestäuber nicht adäquat versorgen und durch die Zugabe von einigen wenigen Samenarten signifikant verbessert werden könnten. Wenn auch im Einzelnen die optimalen Ergänzungen regional variieren können, könnte die Ergänzung mit Pflanzenarten, die funktionell denen, die wir identifizierten, entsprechen, die Wiederherstellung von Ökosystemdiensten, die von einheimischen Bienen geleistet werden, signifikant verbessern. ¨ © 2014 Gesellschaft f¨ur Okologie. Published by Elsevier GmbH. All rights reserved.
Keywords: Pollinator; Bee richness; Bee conservation; Prairie; Iowa; Native plants; Grasslands.
Introduction Ecological restoration of declining and degraded habitats is typically designed for relatively few plant and animal species of concern and has historically focused on recreating botanical compositions and structural features of the non-degraded habitat (Young 2000; Ruiz-Jaen & Aide 2005). More recently, as the field of restoration ecology integrates with the science of conservation biology, restoration of functional aspects of ecosystems and their impact on sustainability of ecosystem services are now receiving equal attention (Devoto, Bailey, Craze, & Memmott 2012; Montoya, Rogers, & Memmott 2012). In practice, however, while restoration of topography, soil and plant diversity as well as phylogenetic diversity promote diversity of some non-target species such as arthropods (Dinnage, Cadotte, Haddad, Crutzinger, & Tilman 2012), in about two-thirds of examined restorations there is little or no data supporting the assumption that higher trophic levels and non-target species will colonize afterwards (Ruiz-Jaen & Aide 2005). Because the colonization of these restorations by such species is dependent on their dispersal to the site and on the availability of all needed resources, the actual impact of restored lands in promoting diversity and sustaining ecosystem functions is likely to be highly variable. In this study, we used known associations of prairie plants and insects to predict how seed mixes of varying plant richness might restore species richness of an important group, pollinators. Seed mixes used to restore land offer an effective way to introduce a diversity of plants to new and existing restorations, but can vary significantly in the species richness of forbs which could, in turn, impact their ability to support and attract higher trophic levels. Seed inclusion in mixes, however, is frequently driven by practical and economic considerations such as germination success, availability, or market demand, often without regard for their ecological role in restorations. Furthermore, restoration projects can have a number of immediate goals other than maximizing diversity across trophic levels, including suppressing invasive species (Skinner, van der Grinten, & Gover 2012), promoting diversity indirectly (Fiedler, Landis, & Arduser 2011) and increasing floral
diversity for the benefit of specific wildlife such as game birds (Draycott 2012), songbirds (Ortega-Álvarez & LindigCisneros, 2012) and butterflies (Shepherd & Debinski, 2005). Here we investigate whether plant species richness in seed mixes is similar to richness in remnant prairies and we model the ability of seed mixes to attract and support bee communities relative to native prairie remnants. Pollinators are one non-target functional group that can benefit from restored habitat (Winfree 2010) and some evidence has shown that restoration can increase pollinator diversity and abundance (Fiedler et al. 2011; Williams 2011). Restorations that improve pollinator diversity are increasingly important in promoting the success and stability of ecosystems (Winfree, Williams, Gaines, Ascher, Kremen 2008; Potts, Biesmeijer, Kremen, Neumann, Schweiger et al. 2010; Garibaldi, Steffan-Dewenter, Winfree, Aizen, & Bommarco et al. 2013) because of declines in bumble bees (Cameron, Lozier, Stange, Koch, Cordes et al. 2011) and other native bees (Burkle, Marlin, & Knight 2013) (but see Bartomeus, Ascher, Gibbs, Danforth, Wagner et al. 2013). Reciprocally, pollinator diversity can help support the success of prairie restorations by providing pollination services to native flowering forbs (Slagle & Hendrix 2009) and to important agricultural products (Winfree et al. 2008). Thus, pollinators that visit and use restored sites will be important to long-term maintenance of plant diversity and community structure. Using remnant tallgrass prairies to empirically measure the association of specific pollinators with particular plant species, we model how plant species included in seed mixes for prairie restoration might help restore pollinator communities. We focus on bee species because they are the dominant pollinators in most ecosystems (O’Toole & Raw, 1991), including the tall grass prairie biome in the central USA, but little work has been done to evaluate and improve mixes specifically for bees (Winfree 2010). First, we characterize the plant species richness of seed mixes compared to remnant prairies and then using models of bee species accumulation, we address two questions about seed mixes: 1) Are plant communities created using seed mixes expected
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to have similar bee richness as remnant prairies? 2) Can we increase the bee richness in plant communities created using seed mixes by selectively adding a few plant species that are visited by more bees in remnant prairies than expected given their abundance regionally or at a site? We hypothesize that seed mixes will not provide adequate resources to attract a richness of bee species equivalent to native prairie remnants because the mixes contain fewer plant species, but that the addition of a few plant species to these mixes will improve their attractiveness to bees.
collection was unrelated to either abundance or species richness of bees collected (all r values, <0.17, all p values, >0.75). At all sites plant abundance and diversity were quantified by directly counting the number of ramets of each forb species in flower in 5 m by 100 m strip plots within the 1 ha plots established for bee sampling. The number of flowering ramets is a reasonably accurate proxy for floral resources on prairies when sampling over large areas at many sites (Hines & Hendrix 2005) because the dominant families on prairies (Apiaceae, Asteraceae and Fabaceae) (see Results) have similar inflorescences with many flowers, a few of which open daily over a number of days. Plant surveys were conducted within ±3 days of each bee sampling at all sites. Flowering forb species were identified using local and regional guides (McGregor, Barkley, Brooks & Schofield 1986; Christiansen & Müller 1999). The original bee data set consisted of 2934 records of 82 bee species on 71 plant species. This was reduced to 2731 records of 70 bee species collected from 54 plants (Appendix A: Table 1) after invasive plants and their associated bees, cleptoparasitic bees and plant species for which no seeds were commercially available were removed. The 12 cleptoparasitic species (42 individuals; about 1.4% of total) were removed prior to analysis because their presence is dependent on not only flower diversity but also specific host species abundance and thus cannot be reliably modeled in this context. When a bee was caught on a plant that was not present in the plant survey an abundance of 1 was assigned to that plant species at that site (see Appendix A: Table 3). This added on average only two plant species and one bee species at each site.
Materials and methods Remnant prairie sampling From 2002 to 2004 we sampled monthly from May through August seven remnant prairies in the northwest one-quarter of Iowa, ranging in size from 10 to 80 ha (Table 1). The bee community was sampled by hand-netting from flowers and inflorescences in two to three 1-ha plots within each site. Sampling was conducted for 1 h in the morning (9 am to 12:30 pm) and again for 1 h in the afternoon (12:30 to 4 pm) because different bee species are active at different times of day (Stephen, Bohart, & Torchio 1969). We divided plots in half along their east-west axes, and the two collectors simultaneously sampled opposite 0.5 ha sides for 15 min, and then switched sides for 15 additional minutes for a total of 1 h sampling. Sampling time was based only upon search time and did not include the time required to handle bees after netting. The flowering species being used by a bee was noted at the time of capture. We conducted bee sampling only in temperatures greater than 15.5 ◦ C. Winds on prairies are highly variable over time and in local space (e.g. within a plot) because of topographical relief. Wind speeds during collecting were generally between 0 and 15 km/h; if winds were greater than 20 km/h collecting was temporarily suspended until wind gusts abated and bees reappeared. Adverse weather conditions prevented sampling at one prairie in August one year and the number of plots sampled differed between years at some sites because of flooding. As a result, sampling varied between sites from a total of 22–26 h. The number of hours of
Database of seed mixes In spring 2012, we identified four seed companies or organizations specializing in local seed for Iowa prairie restorations (Appendix A: Table 2). From each of these suppliers we selected seed mixes designed for prairies of varying types and species richness, or for the Conservation Reserve Program administered by the US Department of Agriculture Farm Service Agency, and we made an effort to cover the spectrum of mix types and diversities available from each. In
Table 1. Summary of site information and statistics of the bee and native plant species community from hand-netting samples at seven Iowa state prairie preserves. Bee abundance and richness values do not include cleptoparasitic species or bees associated with non-native plants. Prairie preserve
County
Size (ha)
Hand-netting sampling (h)
Bee abundance
Bee species richness
Plant species richness
Prairie type*
Anderson Cayler Doolittle Kalsow Kirchner Mori Steele
Emmet Dickinson Story Pocahontas Clay Clay Cherokee
81 65 10 65 65 16 81
26 26 22 26 23 24 24
266 535 501 595 284 260 288
31 39 31 39 38 32 32
39 35 33 34 37 26 34
1 1 2 2 3 1 1
*1 = Mesic prairie; 2 = Pothole prairie complex with seasonal marshes; 3 = Pothole prairie complex with year-round wetlands.
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total we examined 42 seed mixes containing between 4 and 60 species of forbs and a number of grasses. To ensure proper comparison between mixes and remnant prairies, we removed both rare plant species included in mixes but not found in remnant prairies and plant species that bloomed outside of the bee sampling periods. Inclusion of these plant species could unjustifiably underestimate how attractive to pollinators a seed mix would be relative to a remnant prairie. Also, we combined closely related species in mixes that were similar in bloom time and flower characteristics related to pollination (e.g. Aster spp.), typically at the genus level, and we similarly combined these in the empirical data if they were not previously combined because of potential misidentifications in the field (see Appendix A: Table 1). Less than 20% of the database was reduced by grouping species in this manner. Species in the Asteraceae family were most commonly combined because of its high diversity. We do not expect data manipulations to adversely affect our analysis because many of the species that were combined are locally abundant in the specific areas near the four commercial seed suppliers but rare across the greater prairie ecoregion.
Identifying bee plants Bee visitation to plant species is dependent on a number of factors including local plant species abundance, which can affect attractiveness of bees to species, and geographic distribution, which can affect the pool of bees potentially attracted to a plant. Thus, to identify plants in our samples that might be particularly attractive to bee species across many remnant prairies (herein referred to as “bee plants”), we first analyzed the effect of total site abundance, distribution across sites and regional distribution of each plant species on bee richness. Total site abundance was defined as the total number of flowering ramets of a species across all sites and distribution across sites was defined as the total number of sites (out of seven) at which a species occurred. Regional distribution was determined using dot distribution maps and was defined as the total number of counties (out of a possible 1039) in the Great Plains region in which a plant species had been collected (McGregor & Barkley 1977). This analysis focused on the 30 plants identified to species visited by at least three bee species (Appendix A: Table 1) because plants visited by fewer bee species were unlikely to qualify as bee plants. Preliminary analyses using Pearson product-moment correlations to test for relationships between these three predictor variables of abundance showed that the number of sites at which a plant was recorded in our surveys was significantly related to total site abundance of flowering ramets (r = 0.771, p = 0.001) and regional distribution (r = 0.398, p = 0.033), so we dropped number of sites occupied from further analyses. Additionally, number of sites occupied has a small range (1–7) for the more than 50 plants in the analysis compared to over 40 values when the variable total site abundance is used
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which increases the power of the analysis. Total site abundance and regional distribution were not related (r = −0.071, p = 0.678). We used least-square regression analysis to examine the relationship between regional distribution and bee species richness (adjusted R2 = 0.196, p = 0.008) from which we extracted residuals which were then regressed against the total abundance of ramets across all sites. In this latter analysis all plant species outside the upper 95% confidence level were categorized as “candidate bee plants”. To determine if candidate bee plants were more consistently attractive than expected across different sites, we inspected the least-square regression between local plant abundance at a site and number of bees associated with that plant at the site. Candidate bee plants were then elevated to the status of bee plants if 50% or more of the sites for a plant species fell outside the 95% confidence limit.
Model Species accumulation curves model how species richness or diversity changes as sample size increases. These models randomly draw plant species and record how many new bee species are added with the addition of each plant. This is then permutated a number of times to produce a mean species accumulation curve. First, we modeled the accumulation of bee species in each of the seven remnant prairies. Next we modeled the potential accumulation of bee species in each of the 42 mixes. To account for the natural variability in plant species, plant abundance and bee species between prairie remnants, the model selects the plant species in each mix first and then selects a sample from any of the seven prairie remnants that contained that plant. The process continues until all plant species in a mix are chosen and then permutated 1000 times to produce a mean curve of bee accumulation for a given mix. To limit an artificially high accumulation of rare species when selecting across sites, a reduced data set restricted to the 52 bee species occurring in more than one site was used to model the potential accumulation of bees with mixes. To determine how the seed mixes accumulate bee species compared to remnant prairies, we created a mean species accumulation curve and confidence interval using the same procedure for the mixes with the plant species observed in a single prairie chosen from across all prairies. The accumulation for each mix is then overlaid on the 95% confidence interval of all the remnant prairies to determine whether the expected mean bee accumulation for mixes fell within the range of remnant prairies. To determine whether mixes could be amended to improve their suitability for bees, we modeled the accumulation of bees when seed mixes always included the four plant species from our data shown to qualify as bee plants (see Results). We compared the accumulation of bees for seed mixes that were amended with bee plants to the mixes amended with the same number of randomly drawn plant species which
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Table 2. Count and relative abundance of the ten most abundant plant and bee species in hand-netted samples. A) Plant species
Fig. 1. The accumulation of bee species with increasing number of plant species in each of seven prairie remnant preserves sampled in northwest Iowa. Open points indicate type 1 prairies, closed points type 2 and asterisks type 3 (see Table 1).
were added to ensure that mixes maintained the same plant richness as those amended with bee plants. As in previous analyses, a plant was chosen from a random prairie and used to construct bee associations for plants found in each mix; the process was repeated 1000 times to produce a mean species accumulation curve and associated 95% confidence interval envelope. We used a Wilcoxon paired sign test to compare bee species accumulated between the two types of species additions. We used a multiple response permutation procedure (MRPP)–a permutation method that is similar to MANOVA but considered more robust for ecological data–to determine if bee–plant interactions were significantly different between prairies. MRPP uses a distance matrix to compare the similarity within and between groups and determine whether there is significant difference in the interactions observed (McCune and Grace 2002). All analyses were conducted in R v 2.15.1, using the vegan package for MRPP and scripts written by the first author.
Results Samples from remnant prairies contained between 26 and 39 native flowering plant species and between 31 and 39 bee species (Table 1, Fig. 1). Bees were collected on about 60% of the flowering forb species identified in the plant surveys with the other 40% not having any observed visitors. Plant species on which bees were collected by hand-netting were visited by 0-18 bee species at any individual prairie. The 10 most abundant plant species overall in the plant surveys accounted for about 72% of all flowering forb ramets and were dominated by members of the Asteraceae (Table 2). Even though abundances of plants were highly variable between remnants (Appendix A: Table 3), bee–plant associations between remnant prairies did not differ significantly (MRPP, A = 0.003,
Plant species (family)
Number of ramets (% of total)
Zizia aurea (Apiaceae) Pycnanthemum virginianum (Lamiaceae) Anenome canadensis (Ranunculaceae) Ratibida pinnata (Asteraceae) Coreopsis palmata (Asteraceae) Heliopsis helianthoides (Asteraceae) Lathyrus venosa (Fabaceae) Achillea millifolium (Asteraceae) Monarda spp. (Lamiaceae) Dalea purpurea (Fabaceae)
4013 (16.5) 3447 (14.2) 3203 (13.2) 1679 (6.9) 1355 (5.6) 1351 (5.2) 1027 (4.2) 870 (3.6) 836 (3.4) 742 (3.1)
B) Bee species Bee species (family)
Number of bees (% of total)
Melissodes trinodis (Apidae) Bombus griseocollis (Apidae) Andrena ziziae (Andrenidae) Svastra obliqua (Anthophoridae) Halictus ligatus (Halicitidae) Andrena illinoiensis (Andrenidae) Andrena quintilis (Andrenidae) Hylaeus affinis (Colletidae) Augochlorella aurata (Halictidae) Andrena helianthiformis (Andrenidae)
478 (17.3) 309 (11.2) 199 (7.12) 189 (6.8) 188 (6.8) 160 (5.8) 134 (4.8) 99 (3.6) 96 (3.5) 90 (3.3)
p = 0.120). The 10 most common bee species account for 71% of all individuals and were dominated by members of the Andrenidae and Apidae (Table 2). Seed mixes contained an average of 17.6 plant species, approximately half as many as the average for prairies. When reduced to just the plant species observed in remnant prairies, the average was 14.9 species with a range of 4–28. After reducing modeling results to simulations that occurred at least 5% of the time, mixes with up to 20 plant species accumulated between 6.6 and 31.8 bee species which fell within the confidence intervals for the model of bee species accumulation on the remnant prairies (Fig. 2). We identified eight species in remnant samples as candidate bee plants (see Appendix A: Fig. 1). These were Amorpha canescens (Fabaceae), Cicuta maculata (Apiaceae), Coreopsis palmata (Asteraceae), Dalea purpurea (Fabaceae), Heliopsis helianthoides (Asteraceae), Ratibida pinnata (Asteraceae), Solidago rigida (Asteraceae) and Zizia aurea (Apiaceae). Four of these species were classified as bee plants because the bee richness associated with each plant species fell above the upper 95% confidence limit of the regression between bee richness and log-transformed plant abundance in at least half of the sites at which they occurred.
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Fig. 2. The mean accumulation of bee species for the remnant prairies (heavy black line), and the mean accumulation of bees for each of 42 commercial seed mixes (gray lines) across 1000 simulations reduced to plant richness levels occurring in more than 5% of the simulations. Confidence intervals are for the mean across remnant prairies.
Bee plants were A. canescens (5 of 7 sites), D. purpurea (4 of 7 sites), R. pinnata (4 of 7 sites) and Z. aurea (5 of 7 sites). The remaining four species failed the criterion (C. palmata [2 of 6 sites], C. maculata [1 of 4 sites], H. helianthoides [2 of 7 sites] and S. rigida [1 of 6 sites]). The number of candidate bee plant-site combinations outside the 95% CI at different prairies did not differ from random (χ = 2.70, d.f. = 6, p > 0.5). Three of the four bee plant species are among the top 10 most abundant plant species across all prairies (Table 2), but differed widely in abundance between prairies (see Appendix A: Table 3). Seed mixes contained on average only 2.1 of the four bee plants with 24 of the 42 mixes having two or fewer bee plants and only five mixes with all four bee plants. When seed mixes were modeled to ensure they included all four bee plants, the range of bee species accumulated by mixes was 23–31 bee species. Overall, models with amended mixes had significantly more bee species than mixes that were amended with random species (see Fig. 3, mean range (−0.01–11.8), z = 5.64, p = 0.000). Over 60% of the 37 mixes amended with bee plants accumulated five or more bee species than mixes amended with random plants (Fig. 3). Generally, mixes amended with bee plants had smaller confidence intervals in their total bee species richness than mixes amended with random species, indicating that even low-diversity mixes could benefit pollinators with the addition of a few plant species.
Discussion Our results indicate that the restoration of prairie plant diversity using commercially available seed mixes is likely to
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Fig. 3. The change in the mean bee richness for mixes amended with bee plants relative to mixes amended with random plants. Forb mixes were plotted in ascending order of plant richness (mix 1 = 5 species, mix 42 = 28 species). The dotted line indicates no difference between adding random plants or bee plants and the five mixes that contained all four bee plants are indicated on the zero line. Note: Order of mixes is different than Appendix A: Table 2.
benefit native bees (Fig. 2), a non-target group of organisms. Although mixes accumulated fewer total bee species than remnant prairies because they contain less than half of the forb richness (∼48%) (Fig. 2), all of the mixes fall within the confidence interval for bee species accumulations by remnant prairies. Given that relatively few mixes contain the typical richness of plant species of even the poorest native prairie remnant (26–39 species/0.05 ha) (Appendix A: Table 3), it is unlikely that most mixes can support a bee community as rich as a prairie remnant unless more plants are included. Our modeling analysis of amending mixes to increase attractiveness to bee communities indicates that the addition of a relatively few plant species can significantly increase the value of a restoration to a potential bee community. The four species we identified as particularly important (Amorpha canescens, Dalea purpurea, Ratibida pinnata and Zizia aurea) are potential keystone plants for bee communities in many parts of the tall grass prairie ecoregion because they are widely distributed–as revealed in the regional distribution analysis and the number of sites occupied–and are often abundant on prairies (Appendix A: Table 3). It is possible that their wide distribution and high local abundance may contribute to their selection as bee plants and this wide distribution of the bee plants may also imply that they are suitable for many locations throughout the tallgrass prairie region and could be widely used to restorations for bees. Further, as a group these bee plants flower across the blooming season from May (Z. aurea) to September (R. pinnata) and some are known to provide a rich source of pollen because of high flower number in inflorescences and high pollen/ovule ratios (A. canescens and R. pinnata) (Cruden & Miller-Ward 1981) thus making them highly beneficial to bee pollinators. All of these factors indicate that addition of a few plant species will improve bee community richness in restorations. If bee conservation is a direct or indirect goal of the prairie restoration, inclusion of a few key plant species to
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mixes is a cost-effective method to reach that goal when mixes have a relatively low number of plant species (Fig. 3). It is interesting to note that the five mixes that contain all four bee plants were not targeted for pollinators specifically and were devised by the seed companies rather than for the Conservation Reserve Program. Additionally, many of the plant species in “pollinator” mixes are much better suited for butterflies. This suggests much of the habitat that is set aside in various programs could be more beneficial to bees with only a few plant species added at a relatively low cost. It is worth noting that our estimates of bee richness based on hand-netting are likely an underestimation because 38% of the bee species in our remnant sample (27 of 70) are rare (only 1 or 2 individuals) (Appendix A: Table 1), a phenomenon not uncommon in bee diversity studies (Williams, Minckley, Silveira 2001; Potts, Vulliamy, Dafni, Ne’eman, & Willmer, 2003), indicating there are likely many more species at most remnants that were not collected. In addition, the use of pan trap sampling reveals numerous species not caught by hand-netting (Stephen & Rao 2007). Furthermore, some plant species in mixes likely serve as pollen and nectar sources for bee species, but were not represented in our remnants and thus we cannot estimate their contribution to restored prairies. One major assumption of our model is that plants included in mixes will establish and attract bee species in restored sites as they do in native remnants. Plant establishment in restored areas, however, is known to be highly variable (Carter & Blair 2012) and dependent on a myriad of site-specific features of the restored land such as methods used to clear and maintain it (i.e. tilling, burning or herbicides) (Campbell, Hanula, & Waldrop, 2007; Williams, Crone, Roulston, Minckley, Packer, et al., 2010) and land use history (Xu, Wan, Ren, Han & Jiang 2012). Similarly, bee attraction to prairie plant species is density dependent (see Methods: Identifying bee plants) and within our remnant prairies, abundances of species below 200 flowering ramets/ha attracted relatively few bee species. Bee attraction and persistence in a site is a community level phenomenon, not on an individual species level one, as the model treats it. Each bee species may require a particular group of plant species to persist in an environment, a factor we do not attempt to incorporate in the present model. Thus, we might expect highly variable responses in bee abundance, richness and composition in restored sites, particularly small ones. Although our model broadly takes into account the natural variation in plant abundance and attractiveness to bees by sampling across multiple prairies, we note three additional site characteristics (of many) that can affect bee communities in restored sites, but are not included in our model. First, the composition of the assembled bee community in restored areas will be partially dependent on the quality of the surrounding landscape (Hines & Hendrix 2005). Such landscape effects likely explain some of the variation in the rate
of species accumulations seen at prairie remnant preserves (Fig. 1) and the failure of bee plants in our study to attract more bee species than expected at some sites even when relatively abundant. Second, nesting availability is important to support a diverse bee community (Winfree, 2010), but cannot be included in the model because of unknown variation between restorations in their ability to support bee nesting. For example, absence of cavity-nesting bees may indicate a negative effect of fire on the standing dead stems they typically inhabit (Davis et al. 2008) and the presence of cleptoparasitic species (removed in our study) may indicate a healthy bee community (Sheffield, Pinder, Packer, Kevan 2013). Lastly, the size of restorations is not included in our model, but studies of small natural remnants indicate that they may attract and support bee communities as diverse as larger prairies, if their plant community is relatively rich (Davis et al. 2008; Hendrix, Kwaiser, Heard 2010). We would expect these factors to have a significant effect on the potential pool of bee species attracted to the plant species in restorations. While our study provides insights into possible overall species richness of bee communities in restorations, we recognize that empirically determining actual species composition of restorations will reveal additional important details about the effectiveness and management of restorations for bees. This modeling study is meant to provide preliminary insight into whether landscapes restored using standard mixes will be attractive to bee species. Monitoring of restored prairies will be needed to understand better how well the seed mixes being used actually attract pollinators, although our results suggest previously installed restorations and those using these standard mixes or similar ones are benefitting pollinator conservation, if not duplicating bee communities at prairie remnant sites.
Acknowledgments The authors would like to thank K. Kwaiser and K. Gaddis, for field assistance collecting bees and Kristen Chin for helping create the database of mixes. We thank the Center for Global and Regional Environmental Research, Iowa Living Roadway Trust Fund, Iowa Science Foundation, Prairie Biotic Research, and the Department of Biology for funding to SDH. Additional thanks are due to the Iowa Lakeside Laboratory and to the NSF-Postdoctoral Fellowship in Biology for funding to AHT while working on this project.
Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10. 1016/j.baae.2014.11.001.
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