Floral visitation of the invasive stinking ash in western suburban Chicago.
Article Type:
Report
Subject:
Ash (Tree) (Distribution)
Authors:
Aldrich, Preston R.
Brusa, Anthony
Heinz, Cheryl A.
Greer, Gary K.
Huebner, Cynthia
Pub Date:
01/01/2008
Publication:
Name: Transactions of the Illinois State Academy of Science Publisher: Illinois State Academy of Science Audience: Academic Format: Magazine/Journal Subject: Science and technology Copyright: COPYRIGHT 2008 Illinois State Academy of Science ISSN: 0019-2252
Issue:
Date: Jan, 2008 Source Volume: 101 Source Issue: 1-2
Topic:
Event Code: 690 Goods & services distribution Advertising Code: 59 Channels of Distribution Computer Subject: Company distribution practices
Geographic:
Geographic Scope: United States Geographic Name: Chicago, Illinois Geographic Code: 1USA United States

Accession Number:
189833507
Full Text:
ABSTRACT

Ailanthus altissima (the stinking ash) is an invasive tree that has spread to most states in the continental U.S. No formal study has yet documented the Ailanthus pollination ecology. We observed the insects visiting Ailanthus at four sites in a western suburb of Chicago over several weeks during the summer. Numerous insects visited the flowers, with flies and bees most common, though there was significant heterogeneity among sites in the composition of the local pollinator assemblage. Over half of the pollen carried on the legs of large bees was similar to the Ailanthus morphotype pollen. These results suggest generalist pollination mediated by geographically wide-spread insect vectors, which would facilitate range expansion. Moreover, the reliance on both bees and flies may help explain the species' preference for disturbed sites and its ability to expand into northern latitudes. Ants also were frequent floral visitors and potential symbionts, though they are unlikely pollinators of this dioecious species.

INTRODUCTION

The invasive tree Ailanthus altissima Swingle (stinking ash, Tree-of-Heaven, Chinese sumac) is an increasing component of U.S. forests and is a common weed tree in many cities where it is noted for its capacity to thrive in the cracks in concrete and asphalt nearly as readily as at a forest edge (Pan and Bassuk 1986). Its tenacity inspired the book A Tree Grows in Brooklyn (Smith 1943), and later a movie and musical by the same title. A deciduous member of the tropical family Simaroubaceae (Quassia), A. altissima [Mill] Swingle was first imported from China through England in 1784 by William Hamilton, a Philadelphia gardener (Hu 1979). Additional introductions into the west coast are thought to have occurred with Chinese immigrants during the 1800s. Although other species of the genus exist, Ailanthus altissima (hereafter, Ailanthus) has spread to most states in the United States (USDA-NRCS 2008) by following human disturbances (Hu 1979, Huebner 2003), often along transportation right-of-ways (Burch and Zedaker 2003).

Ailanthus presents large pinnately compound leaves with indeterminate growth, often yielding large swooping leaves that suggest its tropical origin (Fig. 1). It incorporates many of the strategies employed by invasive species including (a) early and profuse reproduction (Feret 1973) wherein a single adult can produce a million seed in a year (California Invasive Plant Council 2008), (b) long-distance seed dispersal (Matlack 1987), (c) aggressive clonal reproduction (Miller 2000), and (d) a reliance on high sunlight (Grime and Jeffrey 1965). Moreover, (e) Ailanthus produces toxins that inhibit plant growth and appear to render it unpalatable to many U.S. herbivores (Heisey 1990a, b, De Feo et al. 2003). For a recent review of the biology of Ailanthus altissima see Kowarik and Saumel (2007).

Much less studied are the interactions between Ailanthus and its mutualists, such as pollinators. Some claim that A. altissima is wind-pollinated (Ballero et al. 2003) but the strong fetid odor of its flowers is thought to attract honey bees as well as beetles and other insects (Hu 1979, Miller 1990). In fact, Ailanthus honey is made in some quarters of Europe (Dalby 2000). There it is reported that bee keepers with hives located near large Ailanthus stands produce a smokey, greenish honey that some consider bitter and undesirable, though pleasant once sufficiently aged. The flowers appear to fit a generalist insect pollination syndrome as they are small and actinomorphic with white to yellowish or greenish petals, presented in dense clusters of racemose cymes (Fig. 1) in April through June and into July. The species is dioecious, though hermaphrodites do exist (Gleason and Cronquist 1993). Flowers of both genders emit a strong fetid odor at times compared to burnt peanut butter (California Invasive Plant Council 2008, Global Invasive Species Database 2008), though some descriptions emphasize the male flowers as particularly odoriferous.

Here, we report on the floral visitors of Ailanthus in the western suburbs of Chicago. Information to date on Ailanthus pollination draws largely on anecdotal records and casual observations. Our study provides quantitative information on the putative pollinator assemblage of this invasive species near its northernmost extent in the Midwestern U.S.

STUDY AREA & METHODS

We conducted the study in the Naperville area, a western suburb of Chicago, Illinois, between the months of June and August 2006. The western suburbs are a mosaic of predominantly urban-suburban habitat intermingled with a large network of forest reserves. We selected four roughly 1-hectare patches of forest that contained Ailanthus, with distances between sites ranging from 0.4 to 3 km. Site 1 contained three large (> 10 cm dbh) female Ailanthus residing in contiguous canopy edge habitat adjacent to a parking lot and a major highway. Site 2 was roughly two km away and contained a single, large, freestanding female Ailanthus in a small park of both prairie (mostly non-native species) and forest habitat. Sites 3 and 4 were another km away and only 0.4 km apart in riparian edge habitat adjoining a major road (site 3) and a parking lot (site 4). Both of these sites held several large Ailanthus, (site 3, N = 7; site 4, N = 5), with both males and females present. Note that population size estimates are only approximate since Ailanthus can propagate clonally (Kowarik 1995) and so in several instances it was unclear what was a ramet versus a genet.

Field observations and collections were made as follows. We marked a single, large Ailanthus inflorescence per tree with string and made insect observations and collections at these during a period of 45 minutes to an hour per site between 9 AM and 2 PM. Most time was allotted per site to detailed observations and collections at a single female focal tree, though we also surveyed and collected from other marked inflorescences at each site every 10-15 minutes. Our goal in conducting the study was to produce a list of candidate pollinators for Ailanthus, and since an effective pollinator must visit both male and female trees to move pollen between genders, one should be able to sample either (or both) genders and capture the subset of visitors that are the truly effective pollinators. Some have noted that the male flowers emit a stronger odor than the female flowers (e.g., Global Invasive Species Database 2008) and this might attract a larger assemblage of floral visitors, though the male-specific visitors are of less interest to our study. We visited all of the four sites every two to three days over the course of two months with exceptions made for rainy and windy weather (total hours of observation, 36). We rotated the order in which we visited the sites so as not to conflate site effects with temporal variation in insect activity.

Insects visiting Ailanthus flowers were collected with a net after they were observed interacting directly with the flowers, rather than simply being present in the vicinity or resting on the inflorescence. A few exceptions to this rule were some of the smaller insects that were captured via an aspirator, some directly from the flowers and some from the net following a sweep. All specimens were stored in a freezer until identification. Specimens were pinned, labeled, mounted, and identified down to the family level of classification using two keys (Borror et al. 1989, Romoser and Stoffolano 1998). Visitation rates were calculated for important taxonomic groups (flies, bees, etc.) and a Pearson chi-square (SPSS program) was used to test for differences in visitor classes among the sites.

During identifications we found that several specimens, particularly the larger bees, carried pollen loads on their legs, which were assayed as follows. Pollen was removed from the leg of eleven bees (family Apidae; ten bees from site 1, one bee from site 3) and placed, separately, into microcentrifuge tubes containing Calberla's stain (2 drops of saturated aqueous solution of basic fuchsin, 5 ml glycerol, 10 ml 95% ethanol, and 15 ml distilled water). These were vortexed and examined under a compound microscope. As a control, we examined the treated pollen from Ailanthus and used this morphotype to compare against the pollen carried by the insects. For each sample we determined the frequency of grains that were like and unlike the Ailanthus morphotype with sample sizes ranging from 50 to 77 grains per bee. A Pearson chi-square test was used (SPSS program) to determine if the putative Ailanthus pollen load varied across bees. Note that we also found pollen dusted on many of the other insects, including flies, though it was unclear to what extent this was a byproduct of the net capture process. As a result, these were not quantified.

RESULTS

Flies and bees were the most common insects visiting the Ailanthus flowers. A total of 118 insects were collected representing five orders and more than sixteen families (Table 1, Figure 2). The Dipterans (flies) accounted for nearly half of the collections (48.3%) with Hymenopterans second most abundant overall (32.2%), and roughly 2/3 of these bees and the remaining 1/3 ants. Other orders were rare including Hemiptera (true bugs, 10.2%), Coleoptera (beetles, 7.6%), and Lepidoptera (butterflies, 1.7%).

The composition of the insect communities visiting the Ailanthus flowers varied across the four sites, with bees dominant at one site and flies dominant at two other sites. The single tree at site 2 received very low visitation rates and so it was removed from the formal analysis of site heterogeneity. At site 1, bees comprised a larger fraction of the visitor pool (44.7%) than did flies (23.4%). In contrast, the visitor pools at the other sites were dominated by flies while bees represented only a minor component (site 3: 2.7% bees, 56.8% flies; site 4: 3.7% bees, 77.8% flies). A Pearson chi-square test showed that the bee and fly numbers were significantly different when comparing site 1 with pooled data of the adjacent sites 3 and 4 ([chi square] = 32.78, 1 df, P < 0.001).

Morphotype analysis of the pollen carried by bees indicated that bees were indeed actively collecting Ailanthus pollen, not simply visiting the flowers for nectar or by happenstance. The large bees visiting Ailanthus flowers (predominantly at site 1 with all female Ailanthus) carried on their legs a large percentage (58.5%) of pollen that was indistinguishable from Ailanthus pollen collected from a known source (Table 2). The remaining pollen (41.5%) clearly derived from several other unidentified species. Differences in the ratio of Ailanthus versus non-Ailanthus pollen morphotypes were not significant across bees ([chi square] = 13.26, P = 0.104). Allowing for the fact that the pollen of some other species might appear morphologically similar to that of Ailanthus, the 58.5% is an upper bound on our estimate of the percent of Ailanthus pollen carried by these bees. But assuming that these were indeed Ailanthus pollen grains, we have further promoted the status of bees as effective pollinators of Ailanthus since these large bees carrying Ailanthus pollen were collected visiting female Ailanthus flowers, thereby establishing a male--female link.

DISCUSSION

These data support the notion that Ailanthus is pollinated by a variety of generalist insects, most notably flies and bees. Although these visitation data cannot prove effective pollination by these insects, we have nevertheless circumscribed the list of candidates. This list includes taxa recognized as likely pollinators in less formalized studies of Ailanthus reproduction (e.g., bees noted by Dalby 2000). Moreover our list includes many insect taxa known to be generalist pollinators that associate with other invasive plant species (reviewed by Richardson et al. 2000). Plants that maintain more obligate associations with particular pollinators are more bound to the geography of those pollinators and therefore less likely to become invasive. A partial reliance on fly pollination (myophily) in a north-temperate zone is reasonable given other studies of floral visitation that have shown an increase in the importance of fly pollination with increasing altitude and elevation (reviewed in Kearns 2001). The infestation of Ailanthus in the Chicago area is near the northernmost extent of the range of Ailanthus in the Midwestern U.S., where it reaches into Wisconsin and Michigan but only sparingly with concentrations near Chicago and in Milwaukee and Detroit (USDA--NRCS 2008).

Our list of floral visitors of Ailanthus is largely distinct at the family level from the list of arthropods known to associate with Ailanthus in China. This latter list reported by Siling (1997, cited and described in Zheng et al. 2004) is comprised mostly of natural herbivore pests, not necessarily floral visitors. Some of these associates may serve to keep Ailanthus in check and prevent it from becoming locally invasive. A total of 32 arthropod species are noted as associating with Ailanthus in China: Lepidoptera (12 species of mostly moths and some butterflies), Coleoptera (10 species of beetles), Homoptera and Hemiptera (8 species of true bugs, cicadas, and planthoppers), and Acariformes (2 species of mites). By contrast, these groups form only a small part of our list of floral visitors, with only a single species of butterfly along with a few beetles and true bugs present in our survey of Ailanthus in the Chicago area. The bulk of the floral visitors in our dataset (flies, bees and ants) were not mentioned in the China survey, which is not surprising, geography aside, as the two studies appear to have focused on different modes of insect-plant interactions.

As for flies, despite their generalist behavior and at times inefficient transfer of pollen, flies often contribute to plant reproduction and can rival bees as important pollinators in many circumstances in part due to their sheer ubiquity (Motten 1986, Kearns and Inouye 1994, Kearns 2001, Larson et al. 2001). There are two main types of fly pollination, myophily and sapromyophily. Myophily entails several fly groups that regularly visit flowers for nectar and pollen and can be important pollinators. Families included here are the Anthomyiidae, Bombyliidae, Calliphoridae, Muscidae, Syrphidae, and Tachinidae (Kearns 2001); all but the Bombyliidae were detected at Ailanthus flowers in this study.

The sapromyophilous group of flies, on the other hand, regularly visits dead animals and dung, though they may also visit flowers that emit similar fetid odors, as do the flowers of Ailanthus. If proximity plays a role, the sapromyophilous flies should cross paths with Ailanthus as both have a habit in urban settings of frequenting the less-groomed portions of a city, areas in which it is not uncommon to find garbage lying about (Aldrich, personal observation). In our study, the sarcophagidae (flesh flies) were well-represented at each site. Although their visits may have been largely cases of 'mistaken identity', repeated albeit inefficient visitations may in the balance have led to effective pollination, especially at sites 3 and 4 where bees were less common.

Several factors could explain the among-site heterogeneity of the insect assemblages. First and foremost, the number of sites surveyed was small and so we must be conservative in generalizing the pattern of heterogeneity, though the heterogeneity that we did observe is readily explained. Studies of fly visitation rates often show high spatial heterogeneity in fly numbers and species by site (Herrera 1988, Kearns and Inouye 1994). For example, in our study sites 3 and 4 were near a stream which might have attracted a novel assemblage of insects including more flies compared to the other sites, perhaps due to sewer runoff, goose feces, and various other aquatic sources of carrion and detritus. Another possible factor is the gender differences between sites, as sites 3 and 4 included some male trees that conceivably could have been more attractive to flies, although they would then be less efficient pollinators if they failed to visit females.

The prevailing wisdom has been that bees are an important pollinator of Ailanthus judging from a variety of anecdotal reports and observations (e.g., Miller 1990, Dalby 2000). Our quantitative studies of visitation rates and pollen morphotypes carried on bee legs support this contention. The large bees that we captured visiting Ailanthus flowers carried more Ailanthus morphotype pollen than pollen from other sources (average for 11 bees, 58.5% Ailanthus morphotype pollen). These bees also carried a very similar proportion of Ailanthus morphotype pollen suggesting they were interacting with Ailanthus with some sort of regularity. Moreover, since we captured bees at female trees we are able to establish a male--female connection, further supporting the role of bees as effective pollinators of Ailanthus, not just floral visitors. Bees, like flies, are widespread and important generalist pollinators that likely have facilitated the spread of Ailanthus. However, the decline of bee and other pollinator populations in many areas of the globe (Kearns et al. 1998, Biesmeijer et al. 2006) may lead to a rise in the importance of less efficient yet ubiquitous pollinators such as flies.

Several of the other insect groups visiting the Ailanthus flowers in this study may contribute to pollination (e.g., butterflies, Lepidoptera), though likely not all of these groups. Several of the beetles (Coleoptera), true bugs (Hemiptera), and the ants (Hymenoptera, Formicoidea) may have been casual or predatory visitors rather than pollinators, and some of these groups are well-represented in the survey of natural enemies of Ailanthus in China (Siling 1997, Zheng et al. 2004). Those unable to fly (ants) were further unlikely as pollinators because Ailanthus is dioecious and the insect would have had to travel a large surface distance to the next Ailanthus to affect pollination. These less vagile floral visitors might prove more effective as pollinators should gender determination prove to be more flexible or certain modes of bisexuality more common in Ailanthus than is normally reported.

Even though ants are unlikely pollinators of a dioecious Ailanthus, ants may nevertheless be a symbiont. Ants commonly patrol the leaves of Ailanthus, removing nectar from the flowers and from extra-floral nectaries that occur at the leaf margins and stipules (Aldrich, personal observation). Chemical analysis has shown that the extra-floral nectaries of Ailanthus glandulosa produce sucrose, rhamnose, and several amino acids, mostly serine, threonine, and proline (Bory and Clair-Maczulajtys 1986). These resources may serve as a reward to the ants for protection from herbivores, augmenting Ailanthus' defenses, although ants might also deter potential pollinators as well. The interaction is reminiscent of the symbiosis in the Central American tropics between the bullhorn acacia (Acacia cornigera, Fabaceae) and an ant (Pseudomyrmex ferruginea) that guards the plant against herbivores and in return eats protein nodules from the leaf tips and nectar from petiolar glands, and lives in the hollowed out Acacia thorns (Janzen 1983). Casual observations (Aldrich) of the Ailanthus--ant system in West Lafayette, Indiana revealed that ants behave aggressively toward other insects as they patrol the leaves, and will take up residence in the hollow boles of large adults, in which heart rot is commonplace (Hu 1979).

These data demonstrate that bees, flies, and ants are frequent visitors to the flowers of Ailanthus in the Chicago area. A dependence on generalist pollinators would make colonization of new environments predictably easier, and is a trait manifest by many invasive plants. We have made a case for bees as effective pollinators, and proposed that flies may be important as well although it is conceivable that fly pollination might be less prevalent in lower latitudes. We also submit that ants may be part of a broader generalist symbiosis that includes floral rewards but whose influence may extend into protection from herbivory, further augmenting the chemical defenses possessed by Ailanthus. Such matters deserve further study.

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

ACKNOWLEDGEMENTS

The authors thank C.R.H. Aldrich for field assistance, two anonymous reviewers for comments, and the USDA Forest Service and Benedictine University for support.

received 10/3/07

accepted 3/9/08

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Preston R. Aldrich (1), Anthony Brusa (1), Cheryl A. Heinz (1), Gary K. Greer (2), and Cynthia Huebner (3)

(1) Benedictine University, Lisle, IL 60532

(2) Grand Valley State University, Allendale, MI 49401

(3) USDA Forest Service, Morgantown, WV 26505
Table 1. Insect visitation frequencies at Ailanthus altissima
flowers at four sites in suburban Naperville, IL between
June and August 2006.

Order           Family            Common name           Site 1

Coleoptera      Total             beetles                 3
                Cantharidae       soldier beetles         0
                Cerambycidae      longhorn beetles        0
                Coccinellidae     ladybugs                2
                Other                                     1

Diptera         Total             flies                  11
                Anthomyiidae      flies                   3
                Asilidae          flies                   0
                Calliphoridae     flies                   2
                Helcomyzidae      flies                   0
                Muscidae          flies                   0
                Sarcophagidae     flies                   4
                Syrphidae         flies                   0
                Tachinidae        flies                   1
                Other             flies                   0

Hemiptera       Total             true bugs               8

Hymenoptera     Total             bees / ants            25
                Apoidea           bees                   21
                Andrenidae        bees                    1
                Apidae            bees                    1
                Colletidae        bees                    2
                Halictidae        bees                    2
                Other             bees                   15
                Formicoidea       ants                    4
                Formicidae        ants                    4

Lepidoptera     Total             butterflies             0

TOTAL                                                    47

Order           Family                  Site 2          Site 3

Coleoptera      Total                     1               5
                Cantharidae               1               0
                Cerambycidae              0               1
                Coccinellidae             0               2
                Other                     0               2

Diptera         Total                     4              21
                Anthomyiidae              0               0
                Asilidae                  0               0
                Calliphoridae             0               6
                Helcomyzidae              0               1
                Muscidae                  0               3
                Sarcophagidae             4               5
                Syrphidae                 0               5
                Tachinidae                0               0
                Other                     0               1

Hemiptera       Total                     0               1

Hymenoptera     Total                     1              10
                Apoidea                   1               1
                Andrenidae                0               1
                Apidae                    0               0
                Colletidae                0               0
                Halictidae                0               0
                Other                     1               0
                Formicoidea               0               9
                Formicidae                0               9

Lepidoptera     Total                     1               0

TOTAL                                     7              37

Order           Family                  Site 4          Total

Coleoptera      Total                     0               9
                Cantharidae               0               1
                Cerambycidae              0               1
                Coccinellidae             0               4
                Other                     0               3

Diptera         Total                    21              57
                Anthomyiidae              1               4
                Asilidae                  1               1
                Calliphoridae             0               8
                Helcomyzidae              0               1
                Muscidae                  0               3
                Sarcophagidae             3              16
                Syrphidae                 4               9
                Tachinidae                0               1
                Other                    12              13

Hemiptera       Total                     3              12

Hymenoptera     Total                     2              38
                Apoidea                   1              24
                Andrenidae                0               2
                Apidae                    0               1
                Colletidae                0               2
                Halictidae                0               2
                Other                     1              17
                Formicoidea               1              14
                Formicidae                1              14

Lepidoptera     Total                     1               2

TOTAL                                    27            118

* "Other" indicates specimens that were identified to order
but remained ambiguous at the familial level.

Table 2. Counts of pollen morphotypes collected from the
limbs of bees visiting Ailanthus flowers.
A-morph = Ailanthus-like pollen, N-morph = Non-Ailanthus pollen.

Specimen   A-morph    N-morph    Total

AB007            37         26         63
AB008            33         22         55
AB009            29         27         56
AB031            33         29         62
AB042            30         20         50
AB043            32         20         52
AB053            35         16         51
AB056            50         27         77
AB063            23         31         54
AB077*           30         26         56
AB090            38         19         57

TOTAL           370        263        633

* Collected at site 3, all others collected at site 1.
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