Host plant shifting of the capitulum weevil, Larinus latus (Herbst) (Coleoptera: Curculonidae, Lixinae)

Abstract
Adult and larval host plants of Larinus latus (Herbst 1874), a successful biological control agent, were determined in eastern Turkey. Larinus latus lives on five Onopordum species and uses nine Cardueae species and one Chenopodiaceae as food plants. The most interesting observation is its strict concentration on globe thistle, Echinops sphaerocephalus.

Key words
Larinus latus, host plants, eastern Turkey.

1. Introduction

Phytophagous insects represent a major part of world’s biodiversity. Most hypotheses explaining this extraordinary diversity refer to small body size, specialization on many different microhabitats, short generation time, ability to open up new resources and host plant shifting [Eber et al. 1999] Use of the rostrum for excavating an oviposition site in a plant structure can be seen clearly as a key point in explaining diversity within Curculionoidea [Zwölfer 1975]. The development of a long rostrum in females of Curculionoidea allowed invasion of a new adaptive zone through excavation of oviposition sites in plant parts otherwise not previously available as food sources for immature stages (Anderson 1995). The evolution of host choice and knowledge of how this might affect the speciation process is important for an understanding of this diversity. Considerable attention has been paid to the formation of host races, generally concentrating on host shifts occurring in sympatry [Briese et al. 1996].
The host plant range of Larinus is confined to the tribe Cardueae of the family Asteraceae [Ter-Minassian 1967], [Zwölfer et al. 1971]. Many of the species are highly stenophagous with life histories closely synchronized with those of their host plants [Briese & Sheppard 1992], [Briese et al. 1996], [Sobhian & Fornasari 1994], [Sheppard et al. 1995], [Gültekin et al. 2003].
The weevil Larinus latus (Herbst 1784) is found from the eastern Mediterranean basin to central Asia, where it attacks the capitula of various species of Onopordum thistles. It is the dominant insect exploiting the capitula of this genus [Briese et al. 1994]. As it is restricted to this genus and has the potential to reduce seed production, it was introduced into Australia in 1992 [Woodburn & Briese 1996] for the biological control of three species of Onopordum, considered to be serious pasture weeds following introduction from Europe in the 19^th century [Briese et al. 1990].
Adults feed on the leaves, capitula, and pollen of Onopordum bracteatum Boiss. et Heldr.. Females lay eggs on bracts, in the florets, and in the stems of capitula. The larvae feed on the base of the capitula, florets and seed. Mature larvae produce pupal cells in the margins of capitula and then pupate. New generation adults emerge and migrate to higher altitudes for hibernation. The weevil is univoltine [Gültekin et al. 2003].
Onopordum species are spiny herbs which are biennials, facultative perennials or occasionally winter annuals. The genus Onopordum has a total of seventeen species in Turkey [Davis 1975]. Onopordum acanthium L., Onopordum boissieri Willk. and Onopordum polycephalus Boiss. are common in pastures weeds, and listed by: [Uluğ et al. 1993].

3. Results

Onopordum bracteatum Boiss. et Heldr., Onopordum acanthium L., Onopordum carduchorum Bornm. et Beauverd, Onopordum candidum Nab. and two additional Onopordum species are used as larval host plants by the weevil Larinus latus in eastern Turkey (Table 1). In summer 2004 it was observed that Larinus latus was feeding on globe thistle Echinops sphaerocephalus L. in Sivas province (26 km W of Şarkışla). This locality is 1150 m above sea level. The following plant species were dominant along the highway: Centaurea solstitialis L., Centaurea iberica Trevir et Sprengel, Centaurea sp., Carduus pycnocephalus L., Carduus nutans L., Echinops sphaerocephalus L. and Crambe tatarica Sebeok.. When this place was visited in the first week of June (9.6.2004), 12 specimens of Larinus latus were observed concentrating on three Echinops sphaerocephalus plants (I.: 2 specimens, II.: 4 specimens, III.: 6 specimens). On the second visit, in the third week of June (22.6.2004), plant I. and II. had no Larinus latus, but, number III. had seven individuals. They fed on the stem [Fig. W40_1]: 1-4 and a female tried to open a hole in the capitula-cluster [Fig. W40_1]: 5. Normally, this weevil feeds on the leaves, capitula, and pollen of Onopordum. But, in the association with Echinops sphaerocephalus, adult feeding behaviours changed and they concentrated strongly on the stems for feeding.
In this small plot, the weevil complex was described for the analysis of habitat, diversity and host linkage preliminarily. On Centaurea solstitialis L.: Larinus filiformis Petri 1907, Larinus curtus Hochhuth 1851, and Bangasternus orientalis Capiomont 1874; on Centaurea virgata Lam.: Larinus minutus Gyllenhal 1836; on Centaurea sp.: Larinus nubeculosus Gyllenhal 1836; on Carduus nutans L.: Lixus filiformis (Fabricius 1781), Larinus turbinatus Gyllenhal 1836, and Larinus ochroleucus Capiomont 1874; on Carduus pycnocephalus: Lixus filiformis (Fabricius 1871), Lixus angustatus (Fabricius 1775), and Trichosirocalus horridus (Panzer 1801); on Echinops sphaerocephalus L.: Larinus onopordi (Fabricius 1787) and Larinus latus (Herbst 1784), and on Crambe tatarica Sebeok.: Lixus circumcinctus Boheman 1836, Urodon suturalis (Fabricius 1792), Urodon sp. and Ceutorhynchus sulcicollis Paykull 1800. Here, the dominant weevil species was Larinus filiformis on Centaurea solstitialis and the rarest species Larinus nubeculosus. There was no Onopordum in this habitat.
It was observed that Carduus nutans, Carduus pycnocephalus, Cirsium palustre (L.) Scop., Cirsium vulgare (Savi) Ten., Cirsium sp., Centaurea solstitialis, Centaurea behen L., Centaurea polypodiifolia Boiss., Echinops orientalis Trautv., Arctium minus Bernh. and Beta trigyna Waldst. et Kit. were used as food plants by Larinus latus (Table 1). There are one or two observations concerning feeding on these plants, except Centaurea solstitialis and Beta trigyna. In the Cappadocica region (9 km NE of Ürgüp, 950 m (n = 3) and 19 km NE of Ürgüp, 1020 m (n = 6); 9 June 2004; 22 km E of Avanos, 1180 m (n = 2), 23 June 2004, Nevşehir province), Larinus latus adults were commonly seen on Centaurea solstitialis. In northeastern Anatolia region (42 km S of Köprüköy, 1900 m, 18 June 2002, Erzurum province) Larinus latus adults (n = 9) fed on Beta trigyna leaves and stems, opening round holes.
In this study, the distribution, adult and larval food plant linkage results are summarized in Table 1.

4. Discussion

Larinus latus belongs to a genus of weevils that, in Europe, have co-evolved with thistles of the tribe Cardueae (Asteraceae). All species show high levels of specialization, being oligophagous or monophagous, and feeding as larvae in the capitula of their host plants [Ter-Minassian 1967], [Zwölfer et al. 1971], [Briese 1996]. Larinus latus attacks thistles of the genus Onopordum in the eastern Mediterranean basin and in central western Asia [Briese et al. 1994] and Silybum marianum (L.) Gaertn. in Egypt [Abdel-Moniem 2002]. Host specificity tests of Larinus latus in the field show that it prefers to oviposit on Onoporum acanthium, Onopordum bracteatum and Onopordum tauricum Willd., noting any eggs deposited on capitula of Cynara cardunculus L. and Cynara scolymus L. [Briese et al. 1995]. Even though, under no-choice tests Larinus latus oviposits on Onopordum spp., Silybum marianum, Carduus nutans, Cirsium vulgare and Carthamus lanatus L., but under choice tests the preferred plants are the same except for Carthamus lanatus [Briese et al. 2002]. Zwölfer & Brandl distinguished two morphological and biological different types within the genus Larinus: one with elongated rostrum adapted to piercing the bracts of closed capitula and ovipositing into cavities that were made in these bracts, and the other with short, blunt rostra which exploit the capitulum at a later stage by ovipositing into the florets of the open capitulum. Larinus latus, however, operates over both these functional areas [Zwölfer & Brandl 1989].
Larinus latus is a mobile insect and the adults can easily move to their host plants [Briese et al. 1995]. Gültekin et al. observed that Larinus latus adults of the new generation migrate to higher altitudes for hibernation [Gültekin et al. 2003]. Therefore, this weevil is able to search for and fly to other localities for finding its host plants. On the other hand, most of Larinus latus specimens continued feeding on Echinops sphaerocephalus during two weeks and a female was found drilling a hole into a flowerhead. Furthermore, phytophagous insects have the ability to open up new resources or new ecological niches and to shift host plant [Eber et al. 1999], [Gültekin 2005]. The main flowerhead inhabitant of Echinops sphaerocephalus is Larinus onopordi (Fabricius 1787) which is very common and shows a high population level in Turkey [Gültekin 2006].
Genera, related to Onopordum are Cynara L., Silybum Adans., and Lamira (Cass.) Cass., but Echinops is near the genus Gundelia L. (Dorofeyev, personal communication). Zwölfer et al. supposed a relationship between the tribe Cardueae and associated Larinus species [Zwölfer et al. 1971]: The tribe Cardueae is divided into four subtribes I. Echinopinae, II. Carlininae, III. Carduinae, IV. Centaureinae. Onopordum belongs to the subtribe Carduinae, the genera Cynara and Silybum are related, and Echinops is placed in the subtribe Echinopinae. Although some Larinus species have a narrow host range in Cardueae (species with a thin rostrum mainly prefer the subtribe Centaureinae, for instance) and members of the Larinus vulpes group prefer Echinopinae, some Larinus species use host plants in different genera or subtribes of the tribe Cardueae.
There are only a few investigations dealing with the genus Larinus and the subfamily Lixinae which address especially such biological aspects such as host plants, host plant relationships, biology and behavior. Nevertheless, it is possible to see some extraordinary biological features in the tribe Lixini. For instance, Lixus obesus Petri 1904 completes its generation in seed capsules of Prangos uloptera DC., a new ecological niche for the genus [Gültekin 2005]. The relatively long feeding concentration of Larinus latus on Echinops sphaerocephalus does not confirm whether Echinops is real host. But, the observations showed that this weevil continued feeding on/in the stem of Echinops sphaerocephalus in natural habitat approximately two weeks without trying to find a site with the main host plant despite of its ability to fly.
The reasons why Larinus latus has changed its host plant to the genus Echinops, and also why the Chenopodiaceae genus Beta was utilized for food, can be hypothesized as: 1- hibernated adults could not find the main larval host plant when migrating to lowland areas, 2- lack or absence of main host plant group in the original habitat, 3- asynchrony of host plants and the weevil species, 4- failure to find a suitable adult food resource, 5- searching for a suitable new niche for the immature stages. The behaviour of Larinus latus can also be affected by the similar phenology of flowering in Onopordum and Echinops. The sizes of Onopordum and Echinops capitula are approximately the same, and for these reasons Echinops sphaerocephalus might be selected.
The use of Beta trigyna as adult food by Larinus latus is an unanswered question. Perhaps adults are obtaining water by feeding on Beta trigyna.

Table 1. Distribution and plant association of Larinus latus (Herbst) in eastern Turkey.

5. References

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Anderson R. S. (1995): An evolutionary perspective on diversity in Curculionoidea. - Memoir. Entomol. Soc. Washington 14: 103-114.
Briese D. T. & Sheppard A. W. (1992): Biogeography, host choice and speciation in two Mediterranean species of the weevil genus Larinus. - Proceedings of the VI^th International Conference on Mediterranean Ecosystems (ed. C. A. Thanos), University of Athens, Athens, Greece. 307-314.
Briese D. T., Espiu C. & Pouchot-Lermans A. (1996): Micro-evolution in the weevil genus Larinus: the information of host biotypes and speciation. - Mol. Ecol. 5: 531-545.
Briese D. T., Lane D., Hyde-Wyatt B. H., Crocker J. & Diver R. G. (1990): Distribution of thistles of the genus Onopordum in Australia. - Plant Protection Quarterly 5: 23-27.
Briese D. T., Sheppard A. W. & Reifenberg J. M. (1995): Open-field host specificity testing for potential biological agents of Onopordum thistles. - Biol. Control 5: 158-166.
Briese D. T. (1996): Life history of the Onopordum capitulum weevil Larinus latus (Coleoptera, Curculionidae). - Oecologia 105: 454-463.
Briese D. T., Sheppard A. W., Zwölfer H. & Boldt P. E. (1994): Structure of the phytophagous insect fauna of Onopordum thistle in the northern Mediterranean basin. - Biol. J. Linn. Soc. 53: 231-253.
Briese D. T., Walker A., Pettit W. J. & Sagliocco J. L. (2002): Host-specificity of Candidate Agents for the biological control of Onopordum spp. Thistles in Australia: An assessment of testing procedures. - Biocontrol Sci. and Technol. 12: 149-163.
Davis P. H. (1975): Flora of Turkey and the East Aegean Islands. - Edinburgh University Press, Edinburgh.
Eber S., Knoll S. & Brandl R. (1999): Endophagous insects and structural niches on plants: ecology and evolutionary consequences. - Ecol. Entomol. 24: 292-299.
Gültekin L., Güçlü Ş. & Nikulina O. N. (2003): The life history of capitulum weevil, Larinus latus (Herbst) (Coleoptera: Curculionidae). - NZ. J. Agric. Res. 46: 271-274.
Gültekin L. (2005): New ecological niche for weevils of the genus Lixus Fabricius and biology of Lixus obesus Petri (Coleoptera: Curculionidae, Lixinae) - Weevil News: http://www.curci.de/Inhalt.html, No. 24: 3 pp.
Gültekin L. (2006): Seasonal occurrence and biology of globe thistle capitulum weevil Larinus onopordi (F.) (Coleoptera: Curculionidae) in northeastern Turkey. - Munis Entomology and Zoology 1 (2): 191-198.
Sheppard A. W., Aeschlimann J. P., Sagliocco J. L. & Vitou J. (1995): Below-ground herbivory in Carduus nutans (Asteraceae) and potential for biological control. - Biocontrol Sci. Technol. 5: 261-270.
Ter-Minassian M. E. (1967): Zhuki-dolgonosiki podsemejstva Cleoninae fauny SSSR. Tsvetozhily i stebleedy (triba Lixini). Nauka, Leningrad. (English translation: Weevils of the Subfamily Cleoninae in the Fauna of the USSR. Tribe Lixini. - USDA Agricultural Research Service, Washington, D. C. by Amerind Publishing Co. Pvt. Ltd., New Delhi, 1978).
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Weevil News	http://www.curci.de/Inhalt.html	No. 40	7 pp.	8^th February 2008	ISSN 1615-3472
Gültekin, L. (2008): Host plants of Larinus latus (Herbst 1784) in eastern Turkey (Coleoptera: Curculionidae). - Weevil News: http://www.curci.de/Inhalt.html, No. 40: 7 pp., CURCULIO-Institute: Mönchengladbach. (ISSN 1615-3472).

Province	District	Altitude	Date	Adult / larval host plants	Specimens
Host plant observations (larvae):
Artvin	Şavşat, Çayağazı	1100	22.V.1997	O. bracteatum	4
Bayburt	12 km SW of Aydıntepe	1600	25.VI.1998	O. bracteatum	6
Bingöl	Bingöl env.	1050	2.VI.2001	O. bracteatum	1
Bingöl	Bilaloğlu vill.	1300	3.VI.2001	O. bracteatum	7
Bingöl	40 km S of Bingöl	1400	16.VI.2002	O. bracteatum	1
Elazığ	6 km W of Kovancılar	1020	4.VI.2004	Onopordum sp.	1
Erzincan	Erzincan env.	1200	17.VI.2003	Onopordum sp.	1
Erzurum	Univ. campus	1850	30.VII.1998	O. bracteatum	25 reared
Erzurum	Palandöken Mts.	2200	1.VII.1997	O. bracteatum	1
Erzurum	3 km SW of Ilıca	1850	11.V.2003	O. bracteatum	1
Erzurum	36 km NW of Ilıca	1950	21.VI.2002	O. bracteatum	1
Erzurum	Rizekent	2000	18.VI.1998	O. bracteatum	4
Erzurum	Atlıkonak	1850	12.VII.1997	O. bracteatum	1
Erzurum	Aşkale, Küçükgeçit	1750	8.VIII.1997	O. bracteatum	10
Erzurum	Çayköy	1750	15.VII.1997	O. bracteatum	3
Erzurum	Tepebaşı	1900	15.VII.1997	O. bracteatum	1
Erzurum	Pasinler	1700	17.VII.1996	O. bracteatum	1
Erzurum	Köprüköy, Deliçermik	1650	20.VII.1997	O. bracteatum	2
Erzurum	42 km S of Köprüköy	1900	19.IX.2002	O. bracteatum	7 reared
Erzurum	42 km S of Köprüköy	1900	23.VI.2003	O. bracteatum	2
Erzurum	24 km SE of Horasan	1900	20.VI.2003	O. bracteatum	2
Erzurum	Söğütlü	1750	2.VII.2000	O. bracteatum	5
Erzurum	5-6 km S of Tortum	1880	14.VI.2003	Onopordum sp.	4
Erzurum	Uzundere, Çamlıyamaç	1300	14.VI.2003	O. bracteatum	6
Erzurum	Narman, Kireçli Mt.	2300	2.VII.2000	O. bracteatum	1
Erzurum	Oltu, Sütkans	1800	2.VII.1998	O. bracteatum	2
Gaziantep	İslahiye, Ağabey	550	21.V.2001	Onopordum carduchorum	1
Iğdır	27 km S. of Iğdır	1200	15.VII.2001	O. bracteatum	1
Iğdır	1 km W of Aralık	880	3.VI.2002	O. bracteatum	5
Kayseri	3 km E of İncesu	1020	23.VI.2004	O. bracteatum	6
Kars	21 km E of Horasan	1500	11.VI.1998	O. bracteatum	8
Kars	21 km E of Horasan	1500	4.VII.2000	O. bracteatum	2
Kars	Karakurt	1500	25.VII.1997	O. bracteatum	7
Kars	Şeytangeçmez	1450	2.VI.1999	O. bracteatum	3
Kars	Aras Valley	1450	19.VI.1997	O. bracteatum	2
Malatya	44 km E of Gölbaşı	1550	5.VI.2004	Onopordum sp.	1
Ankara	18 km SE of Şereflikoçkisar	943	23.VI.2005	O. acanthium	6
Bitlis	22 km SW of Bitlis	950	11.VI.2006	O. candidum	2 reared
Host plant observations (adults):
Erzurum	Univ. campus	1850	16.VI.2000	Carduus nutans	1
Erzurum	Univ. campus	1850	1.VI.2002	Carduus nutans	1
Erzurum	Ilıca, Eğerti vill.	1650	18.VI.1998	Cirsium sp.	1
Erzurum	32 km SW of Ilıca	1850	18.VI.1998	Carduus nutans	3
Erzurum	42 km S of Köprüköy	1900	18.VI.2002	Beta trigyna	9
Erzurum	24 km SE of Horasan	1900	20.VI.2003	Cirsium palustre	1
Erzurum	10 km W of Horasan	1700	1.VI.2002	Centaurea behen	1
Erzurum	Söğütlü	1750	14.VI.1999	Cirsium vulgare	4
Erzurum	Aras Valley,39 km N of Hınıs	1796	14.VI.2006	Arctium minus	2
Gümüşhane	3 km NE Torul	1100	20.VI.1998	Carduus pycnocephalus	1
Kars	Aras Valley	1504	22.VI.2007	Echinops orientalis	2
Nevşehir	9 km NE Ürgüp	950	9.VI.2004	Centaurea solstitialis	3
Nevşehir	19 km NE Ürgüp	1020	9.VI.2004	Centaurea solstitialis	6
Nevşehir	22 km E of Avanos	1180	23.VI.2004	Centaurea solstitialis	2
Sivas	26 km W of Şarkışla	1150	9.VI.2004	Echinops sphaerocephalus	12
Sivas	26 km W of Şarkışla	1150	22.VI.2004	Echinops sphaerocephalus	7