Elsevier

Biological Control

Volume 108, May 2017, Pages 16-21
Biological Control

Predicting spillover risk to non-target plants pre-release: Bikasha collaris a potential biological control agent of Chinese tallowtree (Triadica sebifera)

https://doi.org/10.1016/j.biocontrol.2017.02.003Get rights and content

Highlights

  • Bikasha collaris has narrow specificity to the weed Triadica sebifera.

  • Limited feeding occurred in no-choice tests on non-target species, D. fruticosa and G. lucida.

  • Damage, longevity, fecundity by tallow-fed adults was minimal on non-targets.

  • Spillover risk of B. collaris adults was found to be unlikely.

Abstract

Quarantine host range tests accurately predict direct risk of biological control agents to non-target species. However, a well-known direct effect of biological control of weeds releases is spillover damage to non-target species. Spillover damage may occur when the population of agents achieves outbreak densities, depletes the target weed, and some feeding occurs on non-target species. Similar to the assessment of direct risks to non-target species, we assessed the risk of spillover damage to non-target species pre-release. Quarantine experiments were conducted on the flea beetle Bikasha collaris (Coleoptera: Chrysomelidae), a potential biological control agent of Chinese tallowtree, Triadica sebifera, a weed of wetlands, forests, and natural areas in the southeastern U.S.A. Recently emerged, naïve B. collaris adults were fed leaves of T. sebifera (target species), three close relatives that are non-target species (Ditrysinia fruticosa, Gymnanthes lucida, Hippomane mancinella), or water. Adult longevity, egg production, and leaf damage were greatest on the weed and near zero or zero on the non-target species and water control. A spillover event was simulated by transferring adults to non-target species or water after feeding on T. sebifera for 2 or 4 weeks and found similar longevity and egg production as those fed only non-target species or water. These results indicated pre-release that when adults that have fed on T. sebifera are forced to spillover onto the non-target species, there is no risk of damage and that B. collaris will only be able to sustain populations on the target weed.

Introduction

Insect herbivores influence plant performance, regulate plant populations, and shape communities (Maron and Crone, 2006). Classical biological control of weeds, the deliberate introduction of exotic agents to control exotic invasive weeds, seeks to capitalize on these attributes while assisting in the restoration of invaded habitats. Biological control of weeds can be a cost-effective, self-sustaining means of controlling invasive species (van Wilgen et al., 2013). While a few authors have viewed the implementation of biological control of weeds with scepticism and described it as risky (Louda et al., 2003, Simberloff and Stiling, 1996), others claimed it is an underutilized tool that should play a larger role in the control of invasive species in natural areas (Seastedt, 2015). However, biological control should only be implemented with proper assessments of risks and benefits (Hinz et al., 2014, Pemberton, 2000).

Concerns for the safety of biological control focus on two key risks, direct effects where a potential agent may cause significant harm to non-target species and indirect effects where broader ecological impacts may occur (Fowler et al., 2012). These direct effects include transitory damage to non-target species upon which the agent is unable to complete development. Predictions of risks from direct effects are generally determined through no-choice starvation testing which distinguishes hosts from non-hosts (McClay and Balciunas, 2005, Van Klinken, 2000). Although this research has an excellent track record (Balciunas and Smith, 2006), it may overestimate host range and can produce false-positives, excluding otherwise safe agents (Van Klinken, 2000). An approved agent may exhibit a small amount of feeding on a non-target species, and this may be considered acceptable as the agent may be unable to complete development and sustain a population on any species but the target weed. Such direct effects may occur as transient damage in the form of spillover onto non-target species that grow in association with the weed. Distinguishing these short term ephemeral effects from more sustainable non-target damage would be helpful while making decisions pre-release about the relative risk of potential agents. Predicting both direct and indirect risks a priori is a major goal and challenge of weed biological control.

Spillover in weed biological control is a direct effect where a non-target is used after an agent builds up high numbers leading to the collapse of the target weed population (Schooler et al., 2003). While herbivores may commonly restrict their host range to sub-family taxa (e.g., genus) (Forister et al., 2015, Jaenike, 1990, Novotny and Basset, 2005, Novotny et al., 2002), strictly monophagous species may be only rarely available as biological control agents (Sheppard et al., 2005). Consequently, unintended short term spillover onto non-target species may occur especially when oligophagous agents become over abundant and decimate the target weed (Holt and Hochberg, 2001, Lynch et al., 2002). When discovered, this spillover may be of great concern (Dhileepan et al., 2006, Diehl and McEvoy, 1990, Johnson and Stiling, 1998, Rand and Louda, 2004, Stiling et al., 2004). Population outbreaks have been reported following initial release of host specific agents, however these effects are transitory and have not led to long term population level non-target impacts (Catton et al., 2015, Hoddle, 2004a, Hoddle, 2004b, Suckling and Sforza, 2014, Taylor et al., 2007).

Chinese tallow (Triadica sebifera (L.); hereafter ‘tallow’) is one of the most damaging invasive weeds in the southeastern U.S.A., impacting wetlands, forests, and natural areas (Bruce et al., 1997). Classical biological control research of tallow began in 2006 (Wheeler and Ding, 2014) with overseas and quarantine host testing studies resulting in a petition to regulatory authorities requesting field release of a flea beetle, Bikasha collaris (Baly) (Coleoptera: Chrysomelidae) (Huang et al., 2011, Wheeler et al., 2017).

The larvae and adults of B. collaris feed on tallow roots and leaves, respectively. The results of host range studies indicated a high degree of specificity where B. collaris was unable to sustain a population on any non-target species. However, adult no-choice tests showed a limited amount of foliage feeding on two related species of Euphorbiaceae, Ditrysinia fruticosa (Bartram) Govaerts & Frodin and Gymnanthes lucida Sw. Oviposition by B. collaris only occurred on the target weed, tallow and on G. lucida where an average of 4.6 eggs (all non-viable) were produced (Wheeler et al., 2017). Another species of special concern was Hippomane mancinella L., a close relative of tallow and listed as endangered in Florida (Coile and Garland, 2003, Weaver and Anderson, 2010). Our host range research indicated little risk from direct effects by B. collaris on any of these non-targets. However, the risk of spillover damage onto non-targets after B. collaris had fed on tallow was unknown.

Results reported by Wheeler et al. (2017) indicated that, when B. collaris adults had fed on T. sebifera for two weeks, they were able to feed and had extended longevity on two non-target species, D. fruticosa and G. lucida. Possibly, this feeding and extended longevity could be explained by the use of well-fed adults that had previously developed on their primary host on which they acquired sufficient resources to continue to feed after being switched to non-target plants. Thus, we predicted that adult feeding and longevity would decrease if adults were fed on these non-targets without the benefit of prior exposure to T. sebifera.

To examine the risk of spillover pre-release, we compared B. collaris adult performance when they were naïve, or when they were fed tallow for 2 or 4 weeks and then switched to the non-targets in question. These responses were compared with adults fed continuously on tallow and also adults provided with water only. We determined the effects of these manipulations on adult feeding, longevity and oviposition to show pre-release to what extent B. collaris adults could spillover and cause significant and sustained damage on the non-target species.

Section snippets

Insects

In its native range, the flea beetle B. collaris has a temperate to subtropical distribution and was collected in Hubei, Ghizhou, Guangxi, and Hunan provinces ranging from latitudes 31.6°–24.8° North. Quarantine colonies of B. collaris were initiated from two shipments made in November 2008 and October 2009 from Wuhan Botanical Garden, Wuhan, Hubei, China. Upon arrival in the US, the B. collaris collections were housed in the quarantine facility at the Invasive Plant Research Laboratory,

Adult longevity

Mean longevity was significantly greater for naïve B. collaris adult females fed tallow continuously compared with those fed only water or the leaves of non-target species (F4,10 = 15.87; P = 0.0002) (Fig. 1). Naïve adult females (mean (±SEM)) fed tallow lived significantly longer (63.2 ± 10.9 days) compared with those fed only water (2.3 ± 0.3 days), D. fruticosa (5.5 ± 0.3 days), G. lucida (4.0 ± 0.3 days), or leaves of H. mancinella (8.3 ± 6.1 days) (Fig. 1). All naïve adults fed only water or non-target

Discussion

The results presented here confirm previous research which indicated that B. collaris will not sustain populations on the non-target species (Wheeler et al., 2017). Further, this study indicated that populations of B. collaris will not be sustained without continued access to the target weed. Our results showed that egg production is dependent upon sustained adult feeding on tallow leaves. Further, when fed tallow for 2 or 4 weeks and then switched to non-target leaves, they produced no more

Acknowledgments

We thank Lollis, J.A., Steininger, M. S., (USDA-ARS-IPRL) for technical assistance and J. Ding (Chinese Academy of Science) for field assistance. Additionally, voucher collections of these flea beetles are deposited in US National Museum, Washington DC; Entomology Department, and the Florida State Collection of Arthropods, Gainesville, FL. Our quarantine collections were identified morphologically by Dr. Alexander S. Konstantinov, Systematic Entomology Laboratory, National Museum of Natural

References (61)

  • B.L. Bentley

    Extrafloral nectaries and protection by pugnacious bodyguards

    Annu. Rev. Ecol. Syst.

    (1977)
  • E.A. Bernays et al.

    Host-Plant Selection by Phytophagous Insects

    (1994)
  • B. Blossey et al.

    Nontarget feeding of leaf-beetles introduced to control purple loosestrife (Lythrum salicaria L.)

    Nat. Area J.

    (2001)
  • K.A. Bruce et al.

    Introduction, impact on native habitats, and management of a woody invader, the Chinese tallow tree, Sapium sebiferum (L.) Roxb

    Nat. Area J.

    (1997)
  • H.A. Catton et al.

    Nontarget herbivory by a weed biocontrol insect is limited to spillover, reducing the chance of population-level impacts

    Ecol. Appl.

    (2015)
  • T.D. Center et al.

    Field efficacy and predicted host range of the pickerelweed borer, Bellura densa, a potential biological control agent of water hyacinth

    Biocontrol

    (2002)
  • J.A. Coetzee et al.

    Should the mirid, Eccritotarsus catarinensis (Heteroptera: Miridae), be considered for release against water hyacinth in the United States of America?

    Biocontrol Sci. Tech.

    (2009)
  • N.C. Coile et al.

    Notes on Florida's Endangered and Threatened Plant

    (2003)
  • V.G. Dethier

    Mechanism of host-plant recognition

    Entomol. Exp. Appl.

    (1982)
  • P.J. DeVries et al.

    Butterfly exploitation of an ant-plant mutualism: adding insult to herbivory

    J. N. Y. Entomol. Soc.

    (1989)
  • K. Dhileepan et al.

    Temporal patterns in incidence and abundance of Aconophora compressa (Hemiptera: Membracidae), a biological control agent for Lantana camara, on target and nontarget plants

    Environ. Entomol.

    (2006)
  • J.W. Diehl, P.B. McEvoy, Imact of cinnabar moth (Tyria jacobaeae) on Senecio triangularis, a non-target native plant in...
  • EddMapS, Early Detection and Distribution Mapping System. Available from: <http://www.eddmaps.org>, July 11,...
  • H.J. Esser

    A revision of Triadica Lour. (Euphorbiaceae)

    Harvard Pap. Bot.

    (2002)
  • G.P. Fitt

    The influence of a shortage of hosts on the specificity of oviposition behaviour in species of Dacus (Diptera, Tephritidae)

    Physiol. Entomol.

    (1986)
  • M.L. Forister et al.

    The global distribution of diet breadth in insect herbivores

    Proc. Nat. Acad. Sci.

    (2015)
  • S.V. Fowler et al.

    How can ecologists help practitioners minimize non-target effects in weed biocontrol?

    J. Appl. Ecol.

    (2012)
  • M. Heil

    Extrafloral nectar at the plant-insect interface: a spotlight on chemical ecology, phenotypic plasticity, and food webs

    Annu. Rev. Entomol.

    (2015)
  • H.L. Hinz et al.

    Successes we may not have had: a retrospective analysis of selected weed biological control agents in the United States

    Invasive Plant Sci. Manag.

    (2014)
  • M.S. Hoddle

    Restoring balance: using exotic species to control invasive exotic species

    Conserv. Biol.

    (2004)
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