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Assessing the Specificity of a Herbivore on a Plant of Uncertain Phylogenetic Placing: Listronotus Elongatus a Herbivore of Hydrocotyle Ranunculoides

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Assessing the Specificity of a Herbivore on a Plant of Uncertain Phylogenetic Placing: Listronotus Elongatus a Herbivore of Hydrocotyle Ranunculoides Assessing the specificity of a herbivore on a plant of uncertain phylogenetic placing: Listronotus elongatus a herbivore of Hydrocotyle ranunculoides G. Cabrera Walsh & Mariano Maestro BioControl Journal of the International Organization for Biological Control ISSN 1386-6141 BioControl DOI 10.1007/s10526-017-9785-0 1 23 Your article is protected by copyright and all rights are held exclusively by International Organization for Biological Control (IOBC). This e-offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy BioControl DOI 10.1007/s10526-017-9785-0 Assessing the specificity of a herbivore on a plant of uncertain phylogenetic placing: Listronotus elongatus a herbivore of Hydrocotyle ranunculoides G. Cabrera Walsh . Mariano Maestro Received: 13 May 2016 / Accepted: 2 January 2017 Ó International Organization for Biological Control (IOBC) 2017 Abstract Hydrocotyle ranunculoides (Araliaceae) is possibly survive as adults on Hydrocotyle modesta. an aquatic plant native to the Americas and invasive in Results confirm that typical laboratory starvation tests Europe. This work reports laboratory and garden can provide a dependable ranking of physiological studies on the host range of its main natural enemy, the acceptability of different plant species but severely weevil Listronotus elongatus (Hustache) (Coleoptera: overestimate the actual host range of a specialized Curculionidae). The genus Hydrocotyle is in a dis- herbivore. They also indicate that the phylogenetic puted phylogenetic situation such that both Apiaceae criterion for test plant list construction must be and Araliaceae must be included in the test list, but approached cautiously if the phylogeny is uncertain lacking a clear criterion of phylogenetic proximity. or disputed. For this reason three testing instances were applied: no-choice on excised leaves, no choice on functional Keywords Floating pennywort Á Listronotus plants, and a multiple choice garden experiment. A elongatus Á Centrifugal phylogenetic method Á large initial test-plant list was reduced to a smaller list Specificity tests Á Hydrocotyle ranunculoides adjusted by a feeding intensity criterion, survival curves and oviposition levels. Feeding was observed on the excised leaves of 21 out of 36 test plants, but as tests progressed to whole plants L. elongatus showed it Introduction could only develop and thrive on its natural host, and Water pennywort (Hydrocotyle ranunculoides L.f.) is a stoloniferous aquatic perennial that forms dense interwoven mats that float on stagnant or slow moving Handling Editor: S. Raghu. waters. It is native to the Americas, but has become G. Cabrera Walsh (&) Á M. Maestro invasive in the UK, other parts of Europe, and western Fundacio´n para el Estudio de Especies Invasivas Australia (Ruiz-Avila and Klemm 1996; Sheppard (FUEDEI), Bolivar 1559, B1686EFA Hurlingham, et al. 2006). Its rapid and thick growth can block Buenos Aires, Argentina e-mail: [email protected] watercourses, interfering with navigation, flood con- trol, water oxygenation, and other recreational and Present Address: ecological functions. Under suitable conditions it can M. Maestro double its biomass in three days (Ruiz-Avila and Instituto Nacional de Tecnologı´a Agropecuaria, Instituto de Microbiologı´a y Zoologı´a Agrı´cola, Aristizabal s/n, Castelar, Klemm 1996). Buenos Aires, Argentina 123 Author's personal copy G. Cabrera Walsh, M. Maestro Several specialized natural enemies have been agent, could not be strictly applied to put together a identified in southern South America (Cordo et al. test plant list for L. elongatus. The centrifugal 1982; Cabrera Walsh et al. 2013). Among these, phylogenetic method involves a hierarchical order in Listronotus elongatus (Hustache) (Coleoptera: Cur- the exposure of the candidate biocontrol agent to the culionidae) is the most common and widespread plant list, from more to less related plant species herbivore on the plant. It is also apparently the key (Wapshere 1974; Briese 2005; Sheppard et al. 2005). herbivore behind the periodical collapse of H. ranun- It often also includes species in associated niches, and culoides patches in wetlands of the Parana´ Delta in crops or protected species that are sometimes remotely Argentina (Cabrera Walsh et al. 2013). Adults of this related to the target plant, and may consider oviposi- weevil feed on the foliage, and lay eggs inside the tion or other plant uses, as well as feeding (Heard and petioles, from where the larvae bore their way to the van Klinken 1998; Cabrera Walsh et al. 2014). Briese submerged stolons where they complete their (2003) has warned of the need to consider phylogenies development. before taxonomy, because the latter does not neces- Cooperation between CABI-Europe and the FuE- sarily reflect the former. Whatever the procedure to DEI in Argentina (formerly USDA-ARS South Amer- build this test-plant list is, the objective is to obtain a ican Biological Control Laboratory) began in sound, significant group of plants that will challenge September 2009, with the objective of studying the the feeding range of a potential agent in such a way natural enemies and ecology of water pennywort in its that no surprise host shifts or host range expansions native range, and select suitable biocontrol agents. will be observed in the field after release (Marohasy Because of its characteristics, L. elongatus was the 1996; Sheppard et al. 2005). prime natural enemy considered, so its host range was Consequently, it was necessary to include both assessed in the field and the laboratory. However, Apiaceae and Araliaceae sensu lato in the test list, but these studies presented an unusual problem in that the lacking any established criterion to order the plant list genus Hydrocotyle L., traditionally in the Apiaceae, according to phylogenetic proximity. The Apiales has been quite recently placed in the Araliaceae includes more than 3700 species, so it would be (Apiales) (Plunkett et al. 2004), while other genera of impossible to test all, or even a significant part of the the subfamily Hydrocotyloideae were kept in the species in the group (http://taxateca.com). For this Apiaceae, in two new subfamilies, Azorelloideae reason three testing instances were applied. For the (mainly cushion plants) and Mackinlayoideae (found first step excised foliage was exposed to the adult in Australasia) (Lowry et al. 2004; Konstantinova and weevils in petri dishes, because this kind of test is Yembaturova 2010; Liu et al. 2012). quick, easy, and takes up little rearing chamber space. Within the Araliaceae, established intrafamilial Through these tests the large initial test-plant list was relationships do not reflect clades resolved through reduced to a smaller list that was more intensely tested. molecular analyses (Lowry et al. 2004). Molecular This intense testing included comparing functional evidence suggests that the Hydrocotyloideae are a plants to excised foliage and an open garden test, in basally branching, polyphyletic lineage within the which the insects were allowed to access the test plants Apiales, and that the genus Hydrocotyle L. should be on their own volition (see Briese et al. 2002, for a considered a basal taxon for the Apiaceae and the similar use of insects without enclosure). The novelty Araliaceae (Lowry et al. 2001; Nicolas and Plunkett of the procedure is that it involved a widely phyloge- 2009), or even one subgroup within the Apiales that netic criterion, but adjusted by a feeding intensity would include Apiaceae, Araliaceae, Pittosporaceae criterion. This criterion inevitably involved a degree and Myodocarpaceae (Plunkett et al. 2004). Be as it of arbitration (Cruttwell McFadyen 1998). This type may, Hydrocotyle L. was removed from its historical of arbitration is almost always needed in feeding phyletic entourage, and is currently in an isolated preference tests because feeding results are seldom clade with the Australasian genus Trachymene Rudge clear-cut. If specificity were defined as zero feeding on within the Araliaceae (Lowry et al. 2004; Nicolas and any plant species other than the target (even under a Plunkett 2009). Due to this indeterminate phylogeny, starvation setup in the laboratory), it should be con- the so called ‘‘centrifugal phylogenetic method’’, used sidered very rare indeed. However, if specificity were to evaluate the specificity of a potential biocontrol defined as negligible use of another host (for feeding 123 Author's personal copy Assessing the specificity of a herbivore on a plant of uncertain phylogenetic placing or oviposition), then it can be considered quite com- field trips were collected opportunistically for planting mon. Again, however, the border between negligible in flower pots in the laboratory gardens. Finally, Pit- and significant non-host feeding is debatable and tosporum tobira (Japanese pittosporum), one of the arbitrated. In the step-by-step procedure described in only two species
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