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Article

Pollinator Communities of Planted and Feral Pyrus calleryana

Department of Biology, University of Findlay, Findlay, OH 45840, USA
*
Author to whom correspondence should be addressed.
Ecologies 2023, 4(1), 1-10; https://doi.org/10.3390/ecologies4010001
Submission received: 21 October 2022 / Revised: 15 December 2022 / Accepted: 16 December 2022 / Published: 21 December 2022
(This article belongs to the Special Issue Feature Papers of Ecologies 2022)

Abstract

:
Pyrus calleryana was intentionally introduced to North America from east Asia in the early 1900s as rootstock for the edible pear tree, Pyrus communis. It was identified as an ideal decorative, agricultural, and horticultural tree because of its small stature, early spring flowering, fire blight resistance and inoffensive fruits. P. calleryana escaped cultivation and is now considered an invasive species, typically found on roadsides, prairies, and fields. The aim of this study is to characterize pollinator community diversity from planted and feral trees, as well as diversity as it compares to expected communities derived from research-grade iNaturalist observations. Pollinators were collected by hand on planted and feral P. calleryana trees in April 2018–2022. A total of 14 taxa of insect pollinator were collected from P. calleryana flowers, with similar levels of diversity of pollinator taxa collected from planted and feral trees, and Apis mellifera and Andrena spp. the most common taxa observed. The sampled pollinator community did not differ from the expected pollinator communities generated using the iNaturalist data on either the planted or feral P. calleryana.

1. Introduction

Invasive species are a leading cause of global biodiversity loss [1], and it is well documented that they reduce local species diversity while their productivity and population sizes increase [2]. Introduction of species to novel ecosystems has become commonplace, and invasive plants are no exception. These plants are often introduced through the ornamental plant trade, accidental introductions, or seed contamination [3]. Their impacts extend beyond novel species and ecosystem interactions to economic damage with approximately USD137 billion spent each year to control invasive species and prevent their spread [4]. Callery pear (Pyrus calleryana Decne. [Rosales: Rosaceae]) is a highly invasive tree species in North America that escaped from ornamental plantings. The characteristics that made it an ideal ornamental, like disease and herbivory resistance, reproductive traits, and high tolerance of diverse environmental conditions, have also allowed it to grow in a variety of suitable habitats throughout eastern North America [5,6,7].
Since being introduced to the United States as an ornamental in the mid-20th century, P. calleryana has spread quickly throughout the eastern portion of the continent. Escaped, feral trees can be found in wetlands, prairies, roadsides, and abandoned fields, as well as in and around forests [7,8]. Individuals sprout vigorously when cut, and they are known to produce numerous fruits [9] dispersed by a variety of animals, including Starling (Sturnus vulgaris, L.), American Robin (Turdus migratorius, L.), and white-tailed deer (Odocoileus virginianus, Zimmerman) [9,10,11]. Seeds have high survivorship and long-term viability [12] and the trees require full sunlight [11]. The profuse, white flowers range in size from 2.0–2.5 cm across and grow in groups of 5–12 per inflorescence (Figure 1) [8]. The species is self-sterile and requires cross pollination by animals, primarily insects, which is similar to other species in the Rosaceae family [5,13].
While the presence of pollinators is essential to the ability of P. calleryana to reproduce and invade new habitats, it is not known which pollinator species may be attracted to the blooms in its introduced range or the impact the tree has on those pollinator communities. Pollinators of the closely related and commercially important Pyrus communis (L. [Rosales: Rosaceae]) include many species belonging to the order Hymenoptera and family Syrphidae [14]. P. communis, however, tends to have fewer pollinator visitors than domestic apple (Malus domestica (Suckow) Borkh. [Rosales: Rosaceae]), a similar spring-blooming fruit tree from the same family, with a slightly later bloom period [15].
Most insect pollinators that use invasive plants for pollen and nectar tend to be generalist consumers [16], but invasive plants have had contrasting effects on pollinator communities in their introduced ranges [17]. Invasive plant species can disrupt pollinator networks [18,19], yet they can also increase overall carrying capacity [20]. Invasive plants can impact pollinators both directly, such as by providing another food source or by being toxic to the pollinator, and indirectly, by changing the ecosystem or competing against the native plants that the pollinators utilize [21]. Davis et al. [17] demonstrated that sites invaded in Ireland by invasive Japanese knotweed (Fallopia japonica, (Houtt.) Ronse Decr.), and Himalayan balsam (Impatiens glandulifera, Royle) had greater diversity of pollinators, while sites invaded by giant hogweed (Heracleum mantegazzianum, Sommier & Levier), had lower diversity of pollinators. In the US State of Utah, invasive flowering plants salt cedar (Tamarix ramosissima, Ledeb.), white clover (Trifolum repens, L.), and yellow sweet clover (Melilotus officinalis, (L.) Lam.), attracted twice as many pollinators as native flowers, although the pollinators on the invasive flowers were generalists while native flowers had mostly specialist species [20]. When looking at invasive fig-marigold (Carpobrotus acinaciformis, (L.) L. Bolus) and erect pricklypear (Opuntia stricta, Haw.), in northeastern Spain, it was determined that the pollinator community richness was the same for both invaded and non-invaded sample plots [18]. Like the study in Utah, the invasive plants in Spain acted as pollination super generalists and a few generalist pollinators visited the invasive trees exclusively. The impacts of P. calleryana on pollinators are not documented, and because the tree continues to invade open habitats throughout its introduced range [5], it is essential to better understand the implications of the tree’s invasion and management on its associated mutualist pollinators.
To better understand and elucidate these relationships, we seek to identify pollinators that utilize P. calleryana. Additionally, since pollinator populations can be larger and potentially more diverse in managed habitat compared to unmanaged habitat [22,23,24], we seek to understand whether intentionally planted ornamental trees attract the same types of pollinators as feral trees that invade natural and semi-natural landscapes (Figure 2). The bloom period of P. calleryana in northern Ohio typically occurs from mid-April to early May, and common pollinator taxa active during this time include Apis mellifera, L. [Hymenoptera: Apidae]; Lasioglossum spp., Curtis [Hymenoptera: Halictidae]; Megachile spp., Latreille [Hymenoptera: Megachilidae]; Agapostemon spp., Guérin-Méneville [Hymenoptera: Halictidae]; Bombus spp., Latreille [Hymenoptera: Apidae]; Halictus ligatus, Say [Hymenoptera: Halictidae]; and Xylocopa virginica, L. [Hymenoptera: Apidae] [25,26]. We expected to observe these species visiting P. calleryana, and hypothesized different communities of pollinators visiting intentionally planted and escaped, feral trees.

2. Methods

2.1. Study Area

Pollinator surveys were conducted at sites in Hancock and Ashland Counties, Ohio, which are located in the Clayey Till Plain Ecoregion of midwestern United States [27] and are within the Lake Erie/Great Lakes Watershed. Climate is classified as Hot Summer Continental Climate (Dfa) following the Koppen Climate Classification system [28]. The area is characterized by flat, glacially modified topography, with somewhat-poorly and poorly drained soils of the Blount-Pewamo complex (Fine, illitic, mesic Aeric Epiaqualfs and Fine, mixed, active, mesic Typic Argiaquolls) [29] Native vegetative cover is deciduous forest dominated by Acer rubrum, Fagus grandifolia, Quercus spp., and Carya spp., and the current land use is primarily agricultural. A network of roadways connects small cities throughout the region, and urban areas have populations ranging from 200–40,000 people. Our work focused on yards and roadsides of urban and suburban areas in the cities of Findlay (41.0442°, −83.6499°, pop. 39,942 [30]) and Ashland (40.8687°, −82.3182°, pop. 19,282 [30]), Ohio, USA.

2.2. Tree Identification, Selection, and Bloom Period

Within the study areas, locations of P. calleryana trees were identified prior to each field season. We located trees in yards, rights-of-way, fields, and roadways. Because we were interested in understanding differences in pollinator communities between planted and feral trees, we identified trees in manicured yards as intentionally planted and those that invaded unmanaged sites as feral. We excluded trees of uncertain origin, those on private property for which we were unable to obtain permission to sample, and those without branches between 1–2 m from the ground. The number of potential trees for sampling grew each season from 10 trees in 2018 to 29 trees in 2022. The actual number of trees sampled varied over the five years of sampling (Table 1). The available collection days per sample season also varied from year to year due in large part to weather conditions such as wind and precipitation.
In spring of each year, when P. calleryana were in bloom, we randomly selected individual trees from the list of potential trees, stratified by tree type: planted or feral. The bloom period and pollinator sampling season began at approximately 123 growing degree days and lasted 2–3 weeks [31]. This corresponds to mid-April to early May in the study area when weather is characterized by a wide variety of conditions, with average daytime temperatures of 10.7 degrees Celsius, and a range of 4.8 to 16.8 C [32]. Average monthly precipitation for April is 95.8 mm of rain and 22.9 mm of snow. We sampled during the P. calleryana bloom period on clear days with the following conditions: air temperatures greater than 10 degrees C, wind speeds less than 2.24 m/s, and no precipitation.

2.3. Pollinator Sample Collection

To determine pollinator community richness and abundance, insect floral visitors were hand-sampled by one or two technicians between the hours of 1200 and 1600. We used a time-constrained search to visually detect pollinators with a 15-min search for a single observer or 7.5 min with two observers. During the search, flying insects that visited a flower located between 1–2 m in height from the ground were captured in a 50 mL centrifuge tube along with the flower. Technicians would place the tube perpendicular to the floral surface on which the pollinator landed, causing the insect to fly up into the tube. The tube was then capped with the flower it landed on and placed on ice. Pollinators were stored in a laboratory freezer and identified to the lowest taxonomic level possible under a stereomicroscope. Voucher specimens are kept at the University of Findlay Forest Ecology Lab, and remaining specimens are in long-term freezer storage for subsequent studies.

2.4. Expected Pollinator Community Data Acquisition

To determine how well the observed pollinator community from P. calleryana represented overall diversity composition of the region, expected landscape-level community richness was determined using data from iNaturalist, an online community science program that allows naturalists to record and share observations [33]. Research-grade observations of bees and wasps (Apoidea excluding ants, and Vespoidea) from the Clayey Till Plain Ecoregion during the month of April in 2018–2022 were extracted from the database using the R library rinat, version 0.1.8 [34]. 192 records were obtained from the database, and in order to randomize data and ensure the sample size was equivalent to our observed sample, rarefaction was used to subsample the data 100 times with a subsample size (n) equal to the number of individuals collected in field work (n = 57).

2.5. Data Analysis

Pollinator community data, including richness and abundance, were tabulated and summarized using R, version 4.1.2, [35], in RStudio, version 2021.09.2+382, [36]. To compare alpha diversity of observed pollinator communities from planted and feral P. calleryana, the Inverse Simpson Diversity Index [37], was calculated for pollinators from each tree and means were compared using a two-sample t-test. For beta diversity, a multivariate homogeneity of group dispersion test determined that group dispersion was homogenous (p = 0.482), and subsequently, a PERMANOVA [38], was used to determine if pollinator community diversity from planted and feral trees differed. Bray–Curtis distance was used to calculate the distance matrix, and differences among samples was visualized using PCA. A Dufrene-Legendre Indicator Species Analysis [39] was then used to determine the relative importance and statistical significance of each pollinator taxon to planted and feral trees. Beta diversity analysis was conducted using the betadisper {vegan} and adonis {vegan} functions, vegan version 2.5–7 [40] and indicator species analysis was conducted using indval {labdsv} function, labdsv version 2.0-1 [41].
To compare observed and expected pollinator species richness at the gamma level, mean richness from the the 100 rarefied subsamples of iNaturalist data was calculated and compared to total number of species in observed pollinators using a one-sample Wilcoxon test, with mu equal to species richness of the observed data.
To compare observed and expected pollinator communities at the alpha level, a second rarefaction of 100 subsamples of iNaturalist data with n = 2, which is the mean sample size from the field data, rounded to the next integer. Alpha diversity was calculated for each subsample, and these values were compared with those of the field data using a two-sample Wilcoxon test.

3. Results

3.1. Observed Pollinator Community

From 2018–2022, 57 pollinators were collected during 44 sampling periods from 21 P. calleryana sites. Sample size each year was influenced by weather conditions that limited the number of days available for sampling each year. 16 of the sample periods yielded no insects. Of the 28 sample periods where insects were collected, 19 were from planted trees and 9 from feral ones. Species richness was 0.25 species/insect and species density was 2 species/hour for these 28 samples. 14 taxa were identified, and the two most common were A. mellifera and Andrena spp. Other taxa represented by more than one individual were Polistes spp., Latreille [Hymenoptera: Vespidae], Bombus spp.; Megachile spp.; Epalpus signifier, Walker [Diptera: Tachinidae]; and Syrphidae [one individual was identified to species, Helophilus fasciatus, Walker; the second to family] (Figure 3).
The mean number of species per sample was 1.3 with a range of 1–2 species. The diversity of taxa from feral and planted trees, as calculated by the inverse Simpson Index, was 1.23 and 1.28, respectively. These means were not statistically different (p = 0.48), suggesting that diversity was similar among both types of trees. Additionally, no statistical difference in beta diversity of pollinators was detected between planted and feral trees: there was overlap in composition of pollinator communities between planted and feral trees (p = 0.493, Figure 4). Importance values comparing composition of pollinators show that the two most common taxa, A. mellifera and Andrena spp. were identified from both feral and planted trees, but values for these taxa tended to be twice as high on planted trees than feral trees. (Table 2). Taxa identified from feral trees represented 4 insect orders, while those of planted trees represented only 2. The orders unique to feral trees, Hemiptera and Coleoptera, were represented by only one individual each.

3.2. Observed and Expected Community Comparisons

Gamma richness of the expected pollinator communities generated using iNaturalist data was 15.95 species, which is statistically greater than the 14 species observed from P. calleryana (p = 2.51 × 10−15). This includes data from planted and feral trees, which did not host different communities, as demonstrated in the previous analysis. The difference of 1.95 species while statistically significant, is within the range of values, 12–20, from random subsamples of iNaturalist data. Additionally, alpha diversity of the expected pollinator community was 1.91, which is statistically greater than that of the observed data at 1.29 (p = 1.6 × 10−16). When the analysis was conducted with a larger sample size, n = 3, the outcome was similar, with an average diversity index of 2.744.

4. Discussion

Our results show that pollinator communities collected from feral and planted P. calleryana trees were not statistically different. Alpha diversity, as measured by the Inverse Simpson Index, was 1.23 for feral trees and 1.28 for planted trees, which is very low relative to the scale of this index, which ranges from 0–100. Alpha diversity is low because of small sample sizes and the because of dominance of two taxa, A. mellifera and Andrena spp., which were collected from both tree types. The influence of these taxa is reflected in the analysis of Beta diversity, which demonstrated that the insect pollinator communities from feral and planted trees did not differ in composition or abundance of taxa, despite the apparent differences in species lists. Feral trees included a greater number of insect orders, but the difference was not statistically significant, owing to the small number of individuals collected from each of the two orders specific to the feral trees. Insects from the order Syrphidae (e.g., hoverflies) were collected from both tree types, and this reflects other studies that demonstrate that the abundance and richness of Syrphidae are higher in areas with invasive flowering plants than areas with native plants only [42].
At the gamma level, including combined samples from all feral and planted trees, most insect visits to P. calleryana were made up of A. mellifera and Andrena spp. at 43.9% and 24.6%, respectively, during blooming periods from 2018–2022. While the community was dominated by a small number of taxa, a wide assemblage of other species also consumed the flower resources of this species. The total number of taxa collected from P. calleryana during this study was only two species less than the average number of taxa recorded in rarefied subsamples from the iNaturalist database. This difference represents 87.5% of expected taxa, suggesting that feral and planted P. calleryana attract a broad community of pollinators.
The composition of pollinator taxa visiting P. calleryana in northwest Ohio is similar to those identified from its native range. In the Tokai District of Japan, where P. calleryana is a glacial relict population [43], the most common families of insect utilizing P. calleryana resources were Syrphidae, Andrenidae, and Apidae, represented by 29%, 13%, and 9% of the individuals sampled, respectively [43]. The larger proportion of Syrphidae, small insects typically observed hovering over flowers, sampled in Japan could be due to sampling methodology. Makimura et al. [43], used net sampling and longer sampling periods which is an effective method for collecting Syrphidae [44] unlike the hand-sampling strategy used in this study. Despite this difference, the dominance of Apidae and Andrenidae is consistent across native and introduced ranges, and all three taxa, including Syrphids, were present in samples from P. calleryana’s introduced range.
Because pollinator richness from P. calleryana did not differ greatly from expected communities identified from iNaturalist, and because the taxa were similar to pollinator populations in P. calleryana’s native range, we propose there is little or no impact on pollinator richness where P. calleryana invades new sites, whether planted intentionally or feral. However, the presence of Syrphid hoverflies on trees in our study may suggest that P. calleryana could have benefits to non-hymenopteran pollinators. Additional studies are needed to examine this relationship. Generally, it is expected that invasive plant species will negatively affect pollinators if their pollen and nectar resources cannot be exploited or that outcompete native flowering plant species [45]. It is also expected that the extent of the impact of an invasive species on the pollinators will depend on spatial distribution of the invasive plant along with the flight range of the pollinators, and temporal patterns of flowering and seasonal activity of the pollinators [17]. However, previous studies have suggested that invasive plant species have a wide range of species-specific effects on pollinator communities [17,18], making it difficult to predict specific impacts of one invasive plant species on a pollinator community. Recent studies have suggested that insects that demonstrate generalist, or polylectic, feeding behaviors benefit more from invasive plants than those that are considered specialists [42]. The most prevalent species collected during this study were A. mellifera and Andrena spp., both of which are considered polylectic [46,47]. This distribution of pollinators found in this study might be a result of the generalist feeding behavior to enable the utilization of these invasive plant species.
This study represents a first step in understanding the relationship between P. calleryana and insect pollinators in North America. It is acknowledged that the analysis is based on a relatively small sample size. In order to further elucidate this relationship, future studies will be conducted on native flowering species that bloom in the early spring along with P. calleryana to compare the pollinator abundance and diversity. A better understanding of the relationship between the pollinator community and the invasive tree will help in making decisions as to whether these invasive trees can be removed without harming the pollinators that rely on them for early season nutrition.

Author Contributions

Conceptualization, B.J.D.; methodology, B.J.D. and A.L.K.; formal analysis, B.J.D.; field work, P.C., A.N., M.H., A.N.H., D.M. and B.J.D.; species identification, B.J.D.; resources, writing, review and editing: P.C., A.N., M.H., A.N.H., D.M., B.J.D. and A.L.K. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded through internal sources provided by the Department of Biology, University of Findlay.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We thank Johnathon Terry, Reegan Kehres, Bailey Wallace, and Breanna Eads for their assistance with field work. Thanks also to Rae Strobel, Kyle Allor, Kathleen Forner, and Cameron Green for assistance with project development and additional field work. Additionally, we thank Brandan Gray for his assistance identifying pollinators and pinning specimens for long-term storage.

Conflicts of Interest

The authors declare no conflict of interest.

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Figure 1. P. calleryana inflorescence. Flower diameter is approximately 2 cm, with 5–12 flowers per inflorescence. Ben Dolan, University of Findlay.
Figure 1. P. calleryana inflorescence. Flower diameter is approximately 2 cm, with 5–12 flowers per inflorescence. Ben Dolan, University of Findlay.
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Figure 2. Representative planted (left) and feral (right) P. calleryana trees from study areas in northern Ohio. Planted trees were in manicured yards, and feral trees were in unmanaged sites and roadsides, sometimes adjacent to, but not part of, manicured yards. P. calleryana is identifiable in these photos by their profuse, white flowers.
Figure 2. Representative planted (left) and feral (right) P. calleryana trees from study areas in northern Ohio. Planted trees were in manicured yards, and feral trees were in unmanaged sites and roadsides, sometimes adjacent to, but not part of, manicured yards. P. calleryana is identifiable in these photos by their profuse, white flowers.
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Figure 3. Abundance of each pollinator taxon identified from planted and feral P. calleryana. Dominant taxa were European honeybee (Apis mellifera) and mining bees (Andrena spp.), and other taxa included wasps, native bees, hoverflies, and other flies.
Figure 3. Abundance of each pollinator taxon identified from planted and feral P. calleryana. Dominant taxa were European honeybee (Apis mellifera) and mining bees (Andrena spp.), and other taxa included wasps, native bees, hoverflies, and other flies.
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Figure 4. Overlap of planted (triangles) and feral (circles) communities using Principle Components Analysis suggests low turnover and similar composition of taxa on planted and feral trees (p = 0.493).
Figure 4. Overlap of planted (triangles) and feral (circles) communities using Principle Components Analysis suggests low turnover and similar composition of taxa on planted and feral trees (p = 0.493).
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Table 1. Number of P. calleryana sampled each year and the number of days with specified weather conditions for sampling during the bloom period.
Table 1. Number of P. calleryana sampled each year and the number of days with specified weather conditions for sampling during the bloom period.
YearPlanted TreesFeral TreesCollection Days
2018703
2019000
2020212
2021011
20221076
Total19912
Table 2. Dufrene-Legendre Indicator Species Values of taxa collected from planted and feral P. calleryana. None were statistically significant indicators of either tree type.
Table 2. Dufrene-Legendre Indicator Species Values of taxa collected from planted and feral P. calleryana. None were statistically significant indicators of either tree type.
Order: FamilyLower ClassificationPlantedFeral
Hymenoptera: ApidaeApis mellifera, L.0.240.11
Hymenoptera: AndrenidaeAndrena spp., Fabricius0.200.15
Hymenoptera: VespidaePolistes spp., Latreille0.020.06
Diptera: TachinidaeEpalpus signifier, Walker0.020.06
Hymenoptera: MegachilidaeMegachile spp., Latreille0.11
Hymenoptera: ApidaeBombus spp., Latreille0.11
Diptera: SyrphidaeHelophilus fasciatus, Walker0.05
Hymenoptera: MegachilidaeOsmia spp., Panzer0.05
Hymenoptera: HalictidaeHalictus spp., Latreille0.05
Hymenoptera: ApidaeXylocopa virginica, L. 0.11
Hymenoptera: HalictidaeAugochlora pura, Say 0.11
Coleoptera: CoccinellidaeHarmonia axyridis, Pallas 0.11
Diptera: Syrphidaeunknown 0.11
Hemiptera: Cydnidaeunknown 0.11
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MDPI and ACS Style

Dolan, B.J.; Kalkstein, A.L.; Haase, M.; Chernisky, P.; Niese, A.; Hicks, A.N.; Miller, D. Pollinator Communities of Planted and Feral Pyrus calleryana. Ecologies 2023, 4, 1-10. https://doi.org/10.3390/ecologies4010001

AMA Style

Dolan BJ, Kalkstein AL, Haase M, Chernisky P, Niese A, Hicks AN, Miller D. Pollinator Communities of Planted and Feral Pyrus calleryana. Ecologies. 2023; 4(1):1-10. https://doi.org/10.3390/ecologies4010001

Chicago/Turabian Style

Dolan, Benjamin J., Abby L. Kalkstein, Madeline Haase, Paige Chernisky, Alivia Niese, Ashlie N. Hicks, and Dolly Miller. 2023. "Pollinator Communities of Planted and Feral Pyrus calleryana" Ecologies 4, no. 1: 1-10. https://doi.org/10.3390/ecologies4010001

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