Susceptibility of lady beetles (Coleoptera: Coccinellidae) to entomopathogenic nematodes

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Abstract

We investigated differential susceptibility of lady beetles to entomopathogenic nematodes, for two reasons: (1) to estimate potential nontarget effects on natural lady beetle populations, (2) to compare the susceptibility of exotic versus native lady beetle species. We hypothesize that successful establishment of some exotically introduced arthropods may be due, in part, to a lower susceptibility relative to competing native species. In laboratory studies, we compared the pathogenicity, virulence, and reproductive capacity of Heterorhabditis bacteriophora and Steinernema carpocapsae among two native (Coleomegilla maculata and Olla v-nigrum) and two successfully established exotic (Harmonia axyridis and Coccinella septempunctata) lady beetles, and a known susceptible lepidopteran host, Agrotis ipsilon. After 1 and 2 days of exposure to either nematode species, mortality of A. ipsilon was higher than in all lady beetles. Thus, we predict that nematode field applications would have significantly less impact on lady beetle populations than on a susceptible target pest. Additionally, the impact of soil-applied nematodes may be lower on lady beetles than on soil-dwelling hosts because the former spends relatively less time on the soil. Exotic lady beetles were less susceptible to nematode infection than native species. Reproductive capacity data also indicated lower host suitability in H. axyridis, but not in C. septempunctata. Overall, the hypothesis that low susceptibility to pathogens in certain exotic lady beetles may have contributed to competitive establishment was supported (especially for H. axyridis). Additional studies incorporating different hosts and pathogens from various geographic locations will be required to further address the hypothesis.

Introduction

Evaluation of entomopathogen effects on nontarget organisms is an important yet relatively neglected area of study (Hajek and Goettel, 2000). Elucidation of entomopathogen effects on nontarget organisms such as beneficial insects will increase our understanding of a biocontrol agent’s ecology in both natural and agricultural ecosystems, and facilitate effective pest management strategies. Pathogen groups with relatively specific host ranges, such as the nucleopolyhedroviruses (Tanada and Kaya, 1993), are considerably less likely to impact nontarget arthropods compared with those groups that contain wide host ranges. Entomopathogenic nematodes (families Steinernematidae and Heterorhabditidae) include many species with relatively wide host ranges that may suppress a variety of insect pest populations in various orders and families (Grewal et al., 2005, Klein, 1990).

Entomopathogenic nematodes are biological control agents that kill their arthropod hosts through a mutualistic relationship with a bacterium (Xenorhabdus spp. and Photorhabdus spp. for steinernematids and heterorhabditids, respectively) (Poinar, 1990). Infective juveniles (IJs), the only free-living stage, enter hosts through natural openings (mouth, anus, and spiracles), or in some cases, through the cuticle. After entering the host’s hemocoel, nematodes release their symbiotic bacteria, which are primarily responsible for killing the host, defending against secondary invaders, and providing the nematodes with nutrition (Dowds and Peters, 2002). The nematodes molt and complete up to three generations within the host after which IJs exit the cadaver to search out new hosts (Kaya and Gaugler, 1993).

For the most part, entomopathogenic nematodes have been reported to be pathogenic to a number of beneficial insects (predators and parasitoids) under laboratory conditions (Akhurst and Smith, 2002, Georgis et al., 1991, Mráček and Ružička, 1990), but field studies to-date report little or no effect on natural nontarget arthropod populations (Akhurst and Smith, 2002, Bathon, 1996, Georgis et al., 1991). The data, however, are insufficient to make blanket conclusions. Additional research is needed to characterize the impact or potential impact of entomopathogenic nematodes on other biocontrol agents that are important to pest regulation.

Our primary objective was to estimate the potential impact of entomopathogenic nematodes on lady beetles. We determined the innate pathogenicity (ability to cause disease) and virulence (degree of disease-causing power) of entomopathogenic nematodes to four important lady beetle species (Coleoptera: Coccinellidae): the seven spotted lady beetle, Coccinella septempunctata L.; Coleomegilla maculata (De Geer); the multicolored Asian lady beetle, Harmonia axyridis Pallas; and Olla v-nigrum Mulsant. There is a dearth of information on entomopathogenic nematode pathogenicity in lady beetles (Laumond et al., 1979, Mráček and Ružička, 1990), and differential susceptibility among lady beetles has not been previously examined. We measured relative susceptibility of lady beetles to two nematodes, Steinernema carpocapsae (Weiser) and Heterorhabditis bacteriophora Poinar. Both nematodes are ubiquitous, widely studied, and sold commercially on a large scale (Gaugler, 2002, Grewal and Georgis, 1999). To estimate the potential impact of entomopathogenic nematode applications, we compared susceptibility among lady beetle species relative to each other as well as to a known susceptible host, the black cutworm, Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) (Capinera et al., 1988, Levine and Oloumi-Sadeghi, 1992).

The study was conducted under laboratory conditions. Certainly, detection of pathogenicity to a particular host in the laboratory does not necessarily mean that the pathogen impacts or can impact disease prevalence in the host’s natural population; physiological host range does not necessarily equal ecological host range (Federici and Maddox, 1996, Hajek and Goettel, 2000). Nonetheless, laboratory evaluations that include negative or positive controls (a susceptible host) can serve as a valuable starting point for estimating potential impact in natural populations (Hajek and Goettel, 2000).

The susceptibility of H. axyridis to entomopathogenic nematodes compared with the susceptibility of O. v-nigrum is of particular interest because differential susceptibility between the two species to the fungal pathogen Beauveria bassiana (Balsamo) Vuillemin was reported previously (Cottrell and Shapiro-Ilan, 2003). Endemic B. bassiana isolates were substantially more virulent to O. v-nigrum than to H. axyridis (Cottrell and Shapiro-Ilan, 2003). We find the comparison especially interesting because O. v-nigrum is native to North America, and H. axyridis is an introduced species from Asia. H. axyridis was first documented as being released in the US during the early 1900s with continued releases occurring periodically through the 1980s (Gordon, 1985, Tedders and Schaefer, 1994). H. axyridis has since successfully established and become dominant in various row-crop and orchard habitats occupied by native lady beetles (Brown and Miller, 1998, Cottrell and Yeargan, 1998, Michaud, 2002). The success of H. axyridis relative to native species has been attributed to high fecundity (Michaud, 2002), aggressiveness, and size (Cottrell and Yeargan, 1998, Michaud, 2002). We hypothesize that the success H. axyridis in establishing itself is also due to low susceptibility to entomopathogens relative to native lady beetle species. The results of Cottrell and Shapiro-Ilan (2003) support this hypothesis. Our second objective in the present study was to determine if the same trend (i.e., greater susceptibility in native versus exotic lady beetles) exists when examining entomopathogenic nematodes. Additionally, we have expanded the comparison to include the native C. maculata and exotic C. septempunctata. To further assess host suitability, we also compared reproductive potential of the entomopathogenic nematodes in each species of lady beetle and in A. ipsilon.

Section snippets

Nematodes and insects

The nematodes used in this study, S. carpocapsae (Cxrd strain) and H. bacteriophora (VS strain), were isolated near West Helena, Arkansas, USA and Barnesville, Georgia, USA, respectively (Shapiro-Ilan et al., 2003). We purposefully chose nematodes isolated from the southeastern USA to represent populations that occur within the overlapping geographical ranges of the lady beetle species being studied. The nematodes were cultured in parallel in last instar Galleria mellonella (L.) (obtained from

Results

In the virulence assays, no significant difference was detected between trials (F = 0.06; df = 1,105; P = 0.80), and no significant interactions were detected between trial effect and the main effects (F = 0.54; df = 2,105; P = 0.58 for the nematode  trial interaction, and F = 0.19; df = 4,105; P = 0.94 for the trial  insect interaction). Therefore, data from trials were combined in all subsequent analyses. A significant interaction was detected between the main effects (nematode and insect) (F = 20.32; df = 2,104; P < 

Discussion

We predict that nematode field applications would have significantly less impact on the lady beetle species than on a susceptible target pest such as A. ipsilon. Although nematode pathogenicity was detected in the lady beetles, virulence was, overall, substantially lower than in the positive control, A. ipsilon. Unlike with H. bacteriophora, mortality of some of the lady beetle species reached relatively high levels of mortality on the second day after exposure to S. carpocapsae, e.g., greater

Acknowledgments

We thank A. Amis, K. Halat, W. Evans, G. Lathrop, and Roger Laster for technical assistance, J. Dyer for assistance in providing A. ipsilon and B. McCornack for assistance in providing C. septempunctata.

References (39)

  • T.E. Cottrell et al.

    Particle film affects pecan aphid (Homoptera: Aphidae) on pecan

    J. Econ. Entomol.

    (2002)
  • B.C.A. Dowds et al.

    Virulence mechanisms

  • N. Elliott et al.

    Effects of an invading coccinellid on native coccinellids in an agricultural landscape

    Oecologia

    (1996)
  • Ewert, M.A., Chiang, H.C., 1966. Effects of some environmental factors on the distribution of three species of...
  • B.A. Federici et al.

    Host specificity in microbe–insect interactions: insect control by bacterial, fungal, and viral pathogens

    Bioscience

    (1996)
  • R. Georgis et al.

    Effect of steinernematid and heterorhabditid nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) on nontarget arthropods

    Environ. Entomol.

    (1991)
  • R.D. Gordon

    The Coccinellidae (Coleoptera) of America north of Mexico

    J. N. Y. Entomol. Soc.

    (1985)
  • P. Grewal et al.

    Entomopathogenic nematodes

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