Technical Comments

Comment on “Invasive Harlequin Ladybird Carries Biological Weapons Against Native Competitors”

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Science  20 Sep 2013:
Vol. 341, Issue 6152, pp. 1342
DOI: 10.1126/science.1241600

Abstract

Conclusions about the nontarget effects of putatively invasive pathogens should be based on biologically relevant data. We disagree that the research experiments on a microsporidium isolated from Harmonia axyridis conducted by Vilcinskas et al. (Reports, 17 May 2013, p. 862) can explain the decline of native coccinellid species in the absence of such data.

We respectfully disagree that conclusions about invasiveness and population impacts can be drawn from the published study concerning the decline of the seven-spotted ladybeetle, Coccinella septempunctata, as a result of consuming microsporidian-infected eggs of the introduced Asian harlequin lady beetle, Harmonia axyridis (1). The conclusions were based on the results of several laboratory tests. First, C. septempunctata develops infections from injected H. axyridis microsporidia but not from heat-treated spores; second, H. axyridis is not deleteriously affected by infection of the microsporidian pathogen, a conclusion based on observation of adult beetles and on transcriptome data from adult beetles and eggs containing spores; and third, injection of synthetic harmonine does not kill the beetles. These tests were not validated with field collections or feeding bioassays, yet the authors invoke the microsporidium as a “biological weapon” against C. septempunctata and other native ladybird beetles.

Our first concern is that injection of partially purified microsporidian spores bypasses the natural barriers to infection—e.g., the midgut milieu that may or may not stimulate spore germination to initiate infection (2) and immune response in midgut cells (3). C. septempunctata will readily imbibe sugar water (4); therefore, a test of natural response to the microsporidium alone would be to feed isolated spores in a sugar-water suspension, answering the following questions: Is C. septempunctata naturally susceptible to this microsporidium and, if so, how does it respond to infection? Likewise, purified or synthetic harmonine should be fed to the beetles to determine whether ingested harmonine can kill C. septempunctata larvae.

C. septempunctata is Palearctic in distribution (5), and H. axyridis and C. septempunctata are naturally sympatric in Asia (6). It is counterintuitive that a naturally occurring pathogen of H. axyridis only severely affects C. septempunctata in other geographic areas. It is not known whether the Nosema sp. found in H. axyridis has a broad natural host range within the Coccinellidae that might include C. septempunctata and other European species.

In a major study cited by the researchers, Kajita et al. (7) showed mortality of C. septempunctata within 3 days of feeding on H. axyridis eggs. The generation time of microsporidia in the Nosema/Vairimorpha complex is typically 4 to 7+ days (8), with increased spore production occurring after the first sporulation. Indeed, in this study by Vilcinskas et al. (1), which bypassed the normal infection process, the microsporidium performed typically, and mortality occurred at about 2 weeks after inoculation, not within the 3-day period previously reported for egg-feeding. Over many collective years of working with microsporidian species from a variety of insect hosts, including coccinellids, and of evaluating infections in nontarget species in the laboratory and in the field (911), we have observed only one case of early fatal response to microsporidia in a nontarget species, that of the lepidopoteran Hemileuca maia, fed Nosema lymantriae. No spores were produced in these larvae, suggesting a massive immune response and a “dead-end” infection (10). It is possible that early mortality of C. septempunctata fed H. axyridis eggs is a result of naturally produced harmonine (rather than the synthetic harmonine used in the reported experiments), another constituent in the eggs, or a combination of harmonine and another constituent.

Although C. septempunctata will occasionally feed on other arthropods, this species is primarily aphidophagous and fungivorous (12, 13), and the enzootic and epizootic prevalence of Nosema sp. in H. axyridis is unknown. Microsporidia are typically density-dependent pathogens, and some species may, indeed, attain high prevalence in insect populations, but many species are maintained at very low enzootic levels in the host population. Low natural prevalence in H. axyridis would suggest that even if the pathogen has a broad host range, the chance that it might be a major factor in the serious decline of a nontarget species that does not feed primarily on coccinellid eggs is low. It is not reasonable to assert that this microsporidium precipitated the severe decline of several coccinellid species without consideration of the dynamics of the pathogen and the natural feeding behavior of the declining coccinellids in the presence of H. axyridis eggs. H. axyridis is known to be a generalist predator, and the literature contains several reports of high-density populations and unidirectional predation by H. axyridis on native lady beetles (14), with C. septempunctata being particularly susceptible (15). This suggests that direct predation and possibly competition are more likely causes for the decline.

The authors state that H. axyridis is not harmed by the microsporidium. Many adult insects and late larval instars exhibit low mortality and few obvious effects of infection with their naturally occurring microsporidia, and, like the fungi to which they are related, microsporidia can “hide” from the host immune system (3). If, however, as the authors suggest, this species is transmitted transovarially, it is likely that the mortality rate is high in newly hatched infected larvae and/or that egg production is low or hatch rate is reduced (8), effectively removing intensely infected insects from the population.

Microsporidia are of importance as primary pathogens of insects and have the potential to be invasive with the global invasions of their natural hosts. Our studies have shown, however, that the physiological (laboratory) host range of microsporidia is rarely equivalent to the ecological (field) host range (10), and we believe that appropriate and ecologically relevant research is needed before drawing conclusions about the dynamics of any particular host-pathogen system.

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