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Risk to native Uroleucon Aphids (Hemiptera: Aphididae) from non-native lady beetles (Coleoptera: Coccinellidae).

Abstract--Aphids in the genus Uroleucon Mordvilko (Hemiptera: Aphididae) are native herbivores that feed on goldenrod (Solidago spp.) and other Asteraceae in North America. The aphids are potential prey for a wide variety of natural enemies, including native and non-native species of lady beetles (Coleoptera: Coccinellidae). Non-native lady beetles were introduced to aid control of pest aphids in cropland, but some (e.g. Coccinella septempunctata L. and Harmonia axyridis [Pallas]) are known to prey upon Uroleucon aphids in natural and semi-natural settings, raising concerns about their nontarget effects on native aphids. The objective of this study was to estimate non-target risk to Uroleucon aphids from non-native lady beetles. Risk was estimated by evaluating consumption of Uroleucon aphids by lady beetles in no-choice laboratory tests, and by determining incidence of non-native lady beetles within naturally occurring patches of goldenrod and giant sumpweed (Cyclachaena xanthifolia (Nutt.) Fresen.) used by U. nigrotuberculatum (Olive) and U. ambrosiae (Thomas), respectively, in eastern South Dakota during 2009 and 2011. Although lady beetles substantially lowered populations of Uroleucon aphids in no-choice laboratory tests, they were infrequently associated with natural occurrences of the aphids, with incidence comprised of only four native Hippodamia convergens Guerin-Meneville and one non-native C. septempunctata on 185 aphid-infested sample units in relatively small patches of goldenrod and giant sumpweed. Despite consumption of aphids in laboratory tests, the particularly low incidence of lady beetles in field surveys indicates an empirically small risk of their predation on U. nigrotuberculatum and U. ambrosiae under field conditions.

Key words: non-target effects, native aphids, Coccinella, Hippodamia convergens, Solidago, Cyclachaena xanthifolia.


Predatory lady beetles (Coleoptera: Coccinellidae) are associated with biological control of various insect pests more than any other group of predators (Obrycki and Kring, 1998). Accordingly, they have been commonly released for classical biological control of arthropods (Gordon, 1985; Michaud, 2012). Over the last century, at least 179 species of lady beetle have been released in the U.S. and Canada, of which [greater than or equal to]27 species have established, including many generalist aphidophagous species (Gordon, 1985; Michaud, 2012). Two aphidophagous species, Coccinella septempunctata L. and Harmonia axyridis (Pallas) established in North America in the late 20th century (Angalet and Jacques, 1975; Chapin and Brou, 1991). They are now widespread across North America and are considered invasive (Snyder and Evans, 2006; Koch and Galvan, 2008; Michaud, 2012). Both species are intraguild predators of native lady beetles, and H. axyridis is considered a pest of fruit and also a nuisance pest in North America (Snyder and Evans, 2006: Koch and Galvan, 2008). However, both lady beetles contribute fortuitously to biological control of some aphid pests in North America (Koch and Galvan, 2008; Michaud, 2012).

Post-release evaluation of introduced biocontrol species are necessary to assess their effect on non-target taxa (Louda et al., 2003; Simberloff, 2012). For instance, various native, non-pest aphids may potentially be impacted from non-target predation by invasive lady beetles (Rand and Louda, 2006). Indeed, C septempunctata and H. axyridis were observed to prey upon native non-target insects (Schellhorn et al., 2005: Koch et al., 2005: Koch et al., 2006), including native aphids (Hesler and Kieckhefer, 2008; Hesler and Petersen, 2008; Hesler et al., 2009).

Aphids of the genus Uroleucon Mordvilko (Hemiptera: Aphididae) are distributed worldwide, and their host plants are predominantly in the Asteraceae (Blackman and Eastop, 2006). At least 43 Uroleucon species are native to North America (Moran, 1984). In the northern Great Plains, a few species of Uroleucon are moderately common from mid- to late summer in natural and semi-natural habitats, such as prairies, riparian strips, parks and roadsides (Moran, 1984: Hesler and Petersen, 2008; Hesler et al., 2009). These species include Uroleucon nigrotuberculatum (Olive) and U. caligatum (Richards) on goldenrod (Solidago spp.), and U. ambrosiae (Thomas) on giant sumpweed (Cyclachaena xanthifolia [Nutt.] Fresen.) (Olsen, 1971; Moran, 1984; Hesler and Petersen, 2008; Hesler et al., 2009).

Risk of depredation to non-target prey species may be considered a function of the incidence and impact of a predatory species (Andow et al., 1995; Koch et al., 2006). Non-native predators, such as C. septempunctata and H. axyridis, negatively affect native species if they 1) co-occur with native species spatially and temporally (incidence), and 2) negatively affect their population dynamics (impact) (Andow et al., 1995). To date, relatively few studies have assessed the risk to non-target aphids from invasive lady beetles. A recent study by Rand and Louda (2006) in Nebraska found that a native, thistle (Cirsium spp.)-feeding aphid (Bipersona sp.) in prairies was negatively impacted by spillover of native and non-native lady beetles (including C septempunctata) from adjacent agricultural habitats.

Aphids are common pests of field crops, and accordingly a group of native and non-native species of aphidophagous lady beetles is associated with crop aphids in the northern Great Plains (Rand and Louda, 2006; Hesler and Kieckhefer, 2008). This group of aphidophagous lady beetles includes native species, such as Hippodamia convergens Guerin-Meneville, and non-natives C. septempunctata and H. axyridis (Wright and DeVries, 2000: Hesler and Kieckhefer, 2008). All of these lady beetles overlap at least temporally when Uroleucon spp. are present in non-crop habitats (Olsen, 1971; Hesler and Kieckhefer, 2008).

Despite observations of invasive lady beetles preying upon Uroleucon sp. in the north-central United States (Hesler and Kieckhefer, 2008; Hesler and Petersen, 2008; Hesler et al., 2009), the risk from such predation has not been determined. The objective of this study was to estimate risk to Uroleucon aphids from non-native lady beetles by determining incidence of lady beetles on Uroleucon-occupied plants in eastern South Dakota, and by evaluating the acute impact on Uroleucon prey by selected lady beetle species in no-choice laboratory tests.


Laboratory, no-choice feeding tests

To assess acute impact, Uroleucon aphids were confined with lady beetles for 24 hr in laboratory tests. Two invasive lady beetles, C. septempunctata and Harmonia axyridis, and the native species, H. convergens, were tested in 2009 and 2011. Coccinella transversoguttata richardsoni Brown, a native species once widely distributed in North America (Gordon, 1985), was also tested in 2011. Coccinella septempunctata, H. axyridis, and H. convergens were collected from various field crops in 2009 and in 2011 at the Eastern South Dakota Soil and Water Research Farm (ESDSWRF), 2 km north of Brookings, SD, and C. transversoguttata richardsoni was obtained from a laboratory colony of individuals originally collected in Washington state (Hesler et al., 2012). Lady beetles were sorted by species, but not sexed. Species were held separately in clear plastic, ventilated, cylindrical containers (9 cm h x 26 cm diam) at the North Central Agricultural Research Laboratory, Brookings. They were fed soybean aphids and given agar as a source of water for 24 hr in the laboratory (2009 only), and then starved for 24 hr before testing in both years. Five lady beetles per species were then placed in a smaller, clear plastic, square container (11 cm w x 11 cm x 4 cm h) that contained one large or two small flower stem(s) (about 10 cm long) of goldenrod heavily infested with U. nigrotuberculatum (i.e., aphid density occluded apical 8 cm of stems). Aphid-infested goldenrod was obtained from a managed prairie plot at ESDSWRF in 2009 and from an unmanaged area at McCrory Gardens horticultural park in Brookings, South Dakota, in 2011. Stems were placed into the test containers within 1 hr of obtaining them. No moisture source was provided for stems or lady beetles. Stems remained turgid and all lady beetles survived during the test.

Three to eight containers with aphids were tested per lady beetle species. Aphid densities on stems (heavy, moderate, light) were assessed by rating at 24 hr post-release both years to determine impact of confinement with lady beetles. The vast majority of aphids remained on stems over the 24-hr period, even when approached by lady beetles, and the categories of heavy, moderate and light referred to aphid densities on stems that respectively were comparable to, roughly halved, or less than one-third of the density when aphids were initially placed in containers. In addition, lady beetles were observed at 1, 3 and 24 hr after release into containers to determine if their interaction with the aphids changed over time (Barton Browne and Withers, 2002). At each time, lady beetles that were feeding on aphids were tallied in both the 2009 and 2011 tests, and lady beetles present on goldenrod stems (whether feeding on aphids or not) were counted in 201 I. Counts of beetles feeding and counts of those present on stems were summed across individual containers for each species. A Cochran-Mantel-Haenszel test was used to determine whether proportions of lady beetles feeding on aphids at the three sample times were independent of species in 2009 and 2011, and whether proportions of lady beetles present on aphid-infested goldenrod stems at each time was independent of species in 2011 (McDonald, 2009; Zar, 2010). Chi-square tests were used to determine effects of species and sample time on proportion of lady beetles feeding in 2009 and the proportion of lady beetles on stems in 2011 (McDonald, 2009; Zar, 2010).

Field surveys of lady beetles on Uroleucon host plants

The incidence of lady beetles on Uroleucon host plants was assessed by field surveys in August 2009 and August 2011. Several patches of goldenrod and other host plants were scouted for Uroleucon aphids in the summers from 2009 through 2012 in Brookings County, South Dakota, at six locations in or near the city of Brookings. In 2009, abundant populations of predominantly U. nigrotuberculatum with occasional small proportions of U. caligatum (Richards) were found in five patches of goldenrod. A robust population of U. ambrosiae (Thomas) was found in a single patch of giant sumpweed. Uroleucon nigrotuberculatum was also found in a single patch of S. missouriensis Nutt. in 2011. Uroleucon-occupied plants were not found in 2010 and 2012.

Individual patches of plants were sampled on one to five dates, for a total of 16 site-date samples across both 2009 and 2011 (Table 1). Thirteen of the 2009 site samples and the single 2011 sample were taken between late morning and early evening (10 a.m. to 7:30 p.m., sunny, no to moderate wind), and two of the 2009 samples were nocturnal (10:30 to 11:30 p.m., half moon, light wind). Individual stems were flagged so that the same plants were repeatedly sampled during diurnal observations at the ESDSWRF and Joe Huffman Park. Solidago samples within a patch were spaced at least 4 m apart to avoid redundant sampling, as individual plants spread via underground rhizomes (USDA NRCS, 2012). Altogether, including repeated samples, there were 209 instances of sampling plants for lady beetles across both years of the study, with plants infested with aphids in 185 instances.

On each sampling occasion, sample plants were approached slowly and at angle to the sun to avoid casting a shadow and thereby potentially disturbing any lady beetles present, and then stooping beside each plant for approximately one minute to survey for lady beetles. Additional time (1 to 2 mins) was taken to count aphids on plants. Any lady beetle on a sample plant was identified to species on-site, or taken to the laboratory for follow-up identification. Non-lady beetle natural enemies present on sample plants were noted but not counted, and any observed predation on Uroleucon aphids by these other predators was recorded.


Laboratory, no-choice feeding tests

Lady beetles reduced aphid densities on goldenrod stems from heavy to light after 24 hr in both years of testing among all species, except that H. axyridis only reduced aphid densities to moderate levels in 2009. These observations generally supported the hypothesis that lady beetles may acutely impact populations of Uroleucon aphids. Even though aphid densities were reduced over the testing periods, relatively low proportions of lady beetles were observed feeding on aphids at the three sample times each year, ranging from a high of 28% by H. convergens at 1 hr post release in 2009 to three instances of no beetles feeding in 2011 (Figs. 1 and 2). However, relatively high proportions of lady beetles were present on stems in the 2011 test, ranging from a high of 80% for C. septempunctata at 1 hr post-release to a low of 43% for H. axyridis after 24 hr.

The 2009 data did not support the hypothesis that proportions of lady beetles feeding on aphids were equal among sample times for each species ([[chi square].sub.MH] = 12.93, df = 1, P < 0.005). Accordingly, when lady beetles were summed across sample times, proportions differed by species ([chi square] = 8.89, df = 2, P < 0.05), with a low proportion of feeding by C. septempunctata at all sample times compared with a high proportion of feeding by H. axyridis and H. convergens at some sample times (Fig. 1). Correspondingly, proportions of lady beetles summed across species differed among sample times ([chi square] = 12.68, df = 2, P < 0.005), with proportions generally diminishing over time (Fig. l). In 2011, proportions of lady beetles feeding were low overall (0 to 10%) and precluded statistical analysis.

Data from 2011 did not support the hypothesis that proportions of lady beetles present on aphid-infested stems were equal among sample times for each species ([[chi square].sub.MH] = 14.35, df = 1, P < 0.005). Accordingly, proportions of lady beetles on stems summed across species differed among sample times ([chi square] = 14.21, df = 2, P < 0.001), with a general diminution over time (Fig. 2). However, proportions of lady beetles on stems summed across sample times did not differ by species ([chi square] = 7.45, df = 3, P > 0.05).

Field surveys

Uroleucon-occupied stems were present in 185 of the 209 sampling instances, with densities ranging from 3 to 436 aphids per infested stem. Five lady beetles were found among the 185 samples, for a 2.7% incidence that was inconsistent with a hypothesis of high lady-beetle incidence on Uroleucon host plants. Four lady beetles were found individually among plants within a patch of S. missouriensis at the Southbrook Nature Park on 8/I 1/2009, and consisted of one larva of C. septempunctata, and one pupa and two adults of Hippodamia convergens. The larva and adults were feeding on Uroleucon nigrotuberculatum when sampled. An adult H. convergens was also observed on aphid-infested Solidago canadensis L. at Brookings Prairie on 8/27/2009, although it did not feed on Uroleucon aphids during one-minute observation. No ants were observed tending Uroleucon aphids during sampling.

Other natural enemies were observed on Uroleucon-occupied plants. Additional natural enemies observed feeding upon Uroleucon aphids on Solidago spp. included crab (or flower) spiders (Araneae: Thomisidae), flower bugs (Hemiptera: Anthocoridae), green lacewing larvae (Neuroptera: Chrysopidae), predaceous fly larvae (Diptera), and parasitic wasp larvae (evident as light-colored mummified aphids, Hymenoptera: Aphidiidae), and although not quantified, these instances of predation were uncommon. Other predators included ambush bugs (Hemiptera: Phymatidae) and soldier beetles (Coleoptera: Cantharidae), but they were never observed feeding on aphids. Potential predators of Uroleucon aphids on C. xanthifolia included flower bugs, plant bugs (Hemiptera: Miridae), and green lacewings, but these were not observed preying upon aphids in field surveys.


Lady beetles reduced aphid densities on goldenrod stems in 24-hr laboratory tests in this study, indicating that both native and non-native species have potential to acutely impact Uroleucon populations. Although aphid numbers were reduced in the tests, relatively low proportions of lady beetles were feeding at any given observation time. This may simply reflect random sampling during non-feeding periods of grooming and resting, but could also indicate prolonged intervals of prey digestion. The somewhat lower proportion of feeding by C. septempunctata relative to other lady beetles may further indicate that Uroleucon is less accepted as prey by this coccinellid. Aphids generally remained on stems over the 24-hr test period, and relatively high proportions of lady beetles on stems indicated a preference to situate themselves on aphid-occupied stems rather than search elsewhere for alternative prey or attempt to escape the containers. Declining proportions of lady beetles feeding on aphids and present on stems over sample times may have indicated some degree of satiation or paralleled diminishing availability of prey in test containers over the duration of the experiment. Regardless, this latter result emphasized the benefit of making observations of no-choice tests over time to detect time-dependent changes in predator behavior (Barton Browne and Withers, 2002).

In field surveys, the relatively low incidence of lady beetles on Uroleucon host plants was unexpected given that the aphidophagous species tested, although typically associated with agricultural fields, are known to feed on non-pest aphids in non-agricultural habitats (Rand and Louda, 2006; Hesler and Kieckhefer, 2008; Hesler and Petersen, 2008: Hesler et al., 2009). Furthermore, four of the five lady beetle individuals observed were native H. convergens, and only one was the non-native, C. septempunctata. Olsen (1971) suggested that aphids on plants such as goldenrod may serve as alternative food sources for H. convergens during periods of low aphid densities in agricultural crops. In 2009 and 2011, densities of aphid prey in the principal local crops ranged from high in soybean to low and moderate in alfalfa and maize (personal observations), and these same lady beetle species were readily collected from such fields for use in the laboratory tests. Thus, aphid densities in crop fields may have been sufficiently high in 2009 and 2011 to have increased residency of lady beetles in crop fields and consequently lowered their incidence in non-crop areas.

Whereas the field survey demonstrated a very low natural incidence of lady beetles associated with Uroleucon aphids, no-choice laboratory tests demonstrated potential of both native and nonnative lady beetles to have acute, negative impact on populations of these aphids. These contrasting results could have arisen if field surveys underestimated incidence of lady beetles on Uroleucon host plants, no-choice tests exaggerated acute impact of lady beetles on aphid densities, or both effects occurred.

No-choice tests provide an estimate of the potential for acute impact of predators on a prey species, but artificial conditions of laboratory no-choice tests may overestimate this impact for various reasons. First, no-choice tests often overestimate impact because they bring natural enemies and prey into close proximity, thereby simplifying predators' search for prey and bypassing prey-finding steps that may limit discovery and exploitation in the field (van Driesche and Murray, 2004). Although consumption of Uroleucon aphids, and consequent impact, by lady beetles was high under laboratory conditions in the present study, factors such as patchiness of natural prey populations and the lack or masking of prey-finding cues may have limited ability of lady beetles to find Uroleucon prey in the field (Cappuccino, 1988: Genung et al., 2012: Hodek and Evans, 2012).

No-choice tests may also overestimate impact when predators are confined only to non-preferred prey (van Driesche and Murray, 2004). This is especially true for lady beetles, as adults may readily consume a particular aphid species even though it is unsuitable for reproductive success or development (Michaud, 2005). Indeed, although reports have documented that lady beetles feed on Uroleucon aphids (Olsen, 1971: Cappuccino, 1988; Genung et al., 2012), several species, such as U. nigrotuberculatum and U. ambrosiae, are poor or unsuitable prey for survivorship of adult and larval lady beetles, including various Hippodamia spp. (Olsen, 1971) and Harmonia axyridis (Snyder et al., 2000; Kamo and Tokuoka, 2011). In addition, infrequent observations of predation on Uroleucon aphids by predatory taxa besides lady beetles in the present study provided circumstantial evidence that these aphids may generally be non-preferred as prey.

Field surveys might have underestimated incidence of lady beetles on Uroleucon-occupied plants, especially if residency time of lady beetles in a patch was relatively short, as maximum time spent sampling individual stems was 1 min. However, even though timed visual sampling used in field surveys was not calibrated against an absolute measure of lady beetle density in the patches, it is unlikely that underestimation was problematic. First, sample plants were approached carefully to minimize emigration from patches by adult lady beetles or dropping from plants by larvae, and this minimized underestimation at time of sampling. Moreover, predatory lady beetles respond to aphid prey through aggregative and reproductive behaviors (Frazer, 1988; Hodek and Evans, 2012). These responses increase their residency in patches, particularly for immature stages that are confined to individual patches, and thereby increase their probability of being sampled. A range of Uroleucon densities was present in the field that could have potentially provoked aggregation and reproduction by lady beetles. However, detection of only five lady beetles (three adults, one pupa, and one larva) suggested weak aggregative and reproductive responses by lady beetles to Uroleucon-occupied plants that limited their incidence in the field surveys.

Altogether, results of the present study indicate a low risk of predation on U. nigrotuberculatum and U. ambrosiae by lady beetles under field conditions when pest aphids are relatively abundant in nearby crop fields. In particular, risk from non-native lady beetles was even lower, as only one C. septempunctata was observed feeding upon Uroleucon aphids in the field. Low availability of pest aphids can occur acutely or seasonally. However, disturbances that acutely reduce pest aphid levels in crop fields, such as alfalfa cutting or insecticide spraying, typically reduce the numbers of aphidophages also (Summers, 1998; Ohnesorg et al., 2009). Season-long reductions in numbers of pest aphids across an agricultural landscape are unlikely due to the diversity of crops that they may colonize. Indeed, observations over the past several years have indicated that aphid pests are generally present and often abundant in one or more crops in a given year in eastern South Dakota and adjacent areas (Hesler et al., 2005; Hesler and Kieckhefer, 2008), reinforcing the apparently small risk to Uroleucon spp. from predation by aphidophagous lady beetles. Nonetheless, laboratory results of the present study indicated that both native and nonnative species of lady beetles have potential to consume significant numbers of Uroleucon aphids when other prey was not available. Thus, additional monitoring of Uroleucon spp. is warranted in future years when pest aphids may be sparse in crop fields to better estimate risk under such conditions.

Other studies have shown a direct impact of introduced lady beetles, such as C. septempunctata and H. axyridis, on nontarget insects such as monarch butterfly larvae (Schellhorn et al., 2005: Koch et al., 2005; Koch et al., 2006), and nonnative coccinellids have been circumstantially implicated to negatively impact native lady beetles (Snyder and Evans, 2006; Koch and Galvan, 2008). However, relatively few studies have assessed the effects of non-native lady beetles on native, non-target, non-pest aphids (Rand and Louda, 2006). Additional native, non-target aphids remain to be tested and should be the subject of future studies (Hesler and Kieckhefer, 2008; Hesler and Petersen, 2008; Hesler et al., 2009).

Caption: Fig. 1. Proportion of lady beetles feeding on Uroleucon spp. aphids on goldenrod stems at three sample times in laboratory no-choice tests, 2009. n represents the number of lady beetles pooled across individual test containers.

Caption: Fig. 2. Proportion of lady beetles feeding on Uroleucon spp. aphids (gray bars) and present on aphid-infested goldenrod stems (black bars) at three sample times in laboratory no-choice tests, 2011. n represents the number of lady beetles pooled across individual test containers.


Eric Beckendorf, Phil Rozeboom, Sara Haberling, Sara Ackman and Ginger McNickle assisted with laboratory tests and field surveys. Colin Favret graciously identified aphids. Eric Beckendorf, Phil Rozeboom, Marissa Koerlin, Lauren Hesler, Paul J. Johnson, John Losey and Sharon Papiernik graciously reviewed drafts of this paper. This work was supported in part by a grant from the National Science Foundation, award number DRL-0741738, and by base funding under USDA-ARS CRIS Project No. 5447-21220-005-00D.


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Received: 6 May 2013: accepted: 6 June 2013

Louis S. HESLER (1)

USDA-ARS, North Central Agricultural Research Laboratory, 2923 Medary Avenue, Brookings, SD 57006, U.S.A.

(1) E-mail address for correspondence:

Table 1. Sites sampled for Uroleucon spp. of aphids and lady
beetles in Brookings County, South Dakota.

Year           Site (1)            Adjacent
                                   land use

2009       ESDSWRF             agriculture

           Joe Huffman         park, agriculture
           Southbrook          park, agriculture
           Fishback            park, agriculture
           Brookings Prairie   agriculture

2011       McCrory Gardens     park, commercial

Year             Aphid host              Sample dates (2)

2009       Solidago missouriensis    Aug. 3, 10, 14, 17, 27(N)
           Cyclachaena xanthifolia   Aug. 19, 27(N)
           Solidago missouriensis    Aug. 4, 10, 14, 17
           Solidago missouriensis    Aug. 11, 13
           Solidago missouriensis    Aug. 11
           Solidago canadensis       Aug. 27

2011       Solidago missouriensis    Aug. 5

Year        Number of stems       Number of
                sampled        coccinellids (3)

2009       8 each date, 16 N          0
           12 each date               0
           8 each date                0
           10, 20                     4
           35                         0
           30                         1

2011       10                         0

(1) ESDSWRF = Eastern South Dakota Soil and Water
Research Farm, prairie tract.

(2) Dates followed by (N) indicate nocturnal
samples taken (10:30 to 11:30 p.m.).

(3) Aug. 11, Southbrook: 1 larva, Coccinella septempunetata;
1 pupa, 2 adults, Hippodamia convergens. Aug. 27, Brookings
Prairie: 1 adult H. convergens (did not feed during


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Author:Hesler, Louis S.
Publication:Entomologica Americana
Article Type:Report
Geographic Code:1USA
Date:Jan 1, 2013
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