Quantcast

Herbivory in Gingers From Latest Cretaceous to Present

September 30, 2008

By Garcia-Robledo, Carlos Staines, Charles L

INTRODUCTION IT IS suggested that rolled-leaf hispine beetles (Hispinae, Coleoptera) and plants from the order Zingiberales maintained a highly specialized plant-herbivore interaction for >60 My. The evidence supporting this old and conservative interaction are herbivory marks found on leaves of the genus Zingiberopsis (Zingiberaceae) from the latest Cretaceous and early Eocene. This fossil herbivory was described as the ichnotaxon Cephaloleichnites strongii (Hispinae, Coleoptera), based on the assumption that this type of herbivory can be solely attributed to extant rolledleaf beetles. This ichnotaxon has been a key element in several analyses on the origin, radiation and diversification of tropical insect herbivores. In this paper we report feeding patterns equivalent to those described in Zingiberopsis fossils but produced by larvae of Pyralidae and Choreutidae (Lepidoptera) and Anopsilus weevils (Curculionidae, Coleoptera) in four families of extant Zingiberales. We discuss the implications of C. strongii not being a rolled leaf beetle and how this may affect the current knowledge of the co- diversification of rolled-leaf beetles and their host plants from the order Zingiberales.

In their paper Timing the radiation of leaf-beetles: Hispines on gingers from latest Cretaceous to recent, Wilf et al. proposed that rolled-leaf hispine beetles (Hispinae, Coleoptera) and plants from the order Zingiberales maintained a highly specialized plant- herbivore interaction in the new world for >60 m.y. (2000). They concluded this based on feeding tracks present in the leaves of 11 fossil specimens of the genus Zingiberopsis (Zingiberaceae) from the latest Cretaceous and early Eocene (Hickey and Peterson, 1978; Wilf et al., 2000). Wilf et al., assured that these herbivory marks can be solely attributed to rolled-leaf beetles based on its similarity with the herbivory patterns described for hispines feeding on extant Heliconia (Heliconiaceae) (Strong, 1977). Wilf et al. (2000) proposed the ichnotaxon Cephaloleichnites strongii (Hispinae, Coleoptera) for the fossil herbivory (Fig. 1.1, 1.3, 1.5, 1.8).

Since the publication of that paper, the ichnospecies Cephaloleichnites strongii (Hispinae, Coleoptera) has been a key element in several analyses on the origin, radiation and diversification of tropical insect herbivores (McKenna and Farrell, 2006; GomezZurita et al., 2007). In a study of the herbivore communities in extant Zingiberales from Central and South America, we found that the fossil herbivory formerly attributed only to hispine beetles can be also produced by other extant insect herbivores. Here we report feeding patterns equivalent to those described in Zingiberopsis fossils but produced by Lepidoptera and Curculionidae in four families of extant Zingiberales.

METHODS

This study was performed in April 2007 at La Selva Biological Station, a tropical rain forest in Costa Rica, Central America (10[degrees]26′N, 84[degrees]00′W) and in March 2006 in South America, in a tropical montane forest in the Peruvian Andes, Municipio de Aguas Calientes, at 2,400 m (13[degrees]09′S, 72[degrees]32′W). Larvae of Lepidoptera feeding on expanded leaves of Zingiberales were collected at La Selva Biological Station (Table 1). Larvae were brought to the laboratory and individually fed 10 X 10 cm of expanded leaf from their host plant. Larvae from the family Pyralidae feed on leaves covered with leaf litter (McCoy 1984). Therefore, in the herbivory trials involving pyralids, leaves were offered covered with a piece of leaf litter collected from the top of the leaves of the host plant. The feeding patterns were recorded after 48 hours.

In the Municipio de Aguas Calientes, Peru, we collected curculionid beetles feeding on young unexpanded leaves of Canna bangii Kraetzl 1912. (Cannaceae, Zingiberales) (Table 1). To determine the characteristics of the damage produced on the leaf blade by curculionids, we offered one 1.5 x 1.5 cm section of fresh C. bangii leaf tissue to each weevil. After 12 hours, we recorded the shape of the damage produced on each leaf section. Finally, we compared the herbivory patterns observed in the laboratory with the patterns produced by hispine and non-hispine herbivores in nature.

RESULTS

In a tropical rain forest in Costa Rica, early instars of Pyralidae and Choreutidae (Lepidoptera) feed on expanded leaves of Heliconiaceae, Marantaceae and Zingiberaceae (Fig. 1.2, 1.4, 1.7, 1.9). In a tropical montane forest in Peru, Anopsilus Kirsch, 1869 weevils (Curculionidae) feed on young rolled leaves of Canna bangii (Cannaceae) (Figs. 1-6). In the laboratory, both lepidopterans and curculionids produced herbivory marks equivalent to those described in Zingiberopsis (Fig. 1) (Wilf et al., 2000). Lepidoptera and Curculionidae removed leaf-tissue in linear strips between parallel veins, leaving the epidermis intact. The damage may be bordered by dark reaction tissue and the terminations of the strips are asymmetrically rounded (Figs. 1.2, 1.4, 1.6, 1.7, 1.9). The herbivory marks observed in the laboratory were equivalent to those produced in nature by Anopsilus weevils and first instar larvae of Pyralidae and Choreutidae.

The relative frequency of hispine vs. non-hispine damage was highly variable among the four species of Zingiberales included in this study. In Canna bangii (Cannaceae) no hispine beetles were recorded. Therefore all the herbivory observed in the field could be attributed to Anopsilus weevils. In Calathea crofalifera (Marantaceae) herbivory by both Choreutidae and Hispinae cooccurred in most of the leaves. In Heliconia (Heliconiaceae) and Renealmia (Zingiberaceae), most of the herbivory observed was produced by hispine beetles. Damage by pyralids was restricted to areas where the host leaves were covered by leaf litter.

DISCUSSION

Our results suggest that hispine beetles are not the only herbivores able to produce the herbivory pattern described by Wilf et al. (2000) in extant Zingiberales. A question that arises from our results is how probable it is that the Pyralidae, Choreutidae and Curculionidae are the actual culprits of the herbivory damage in Zingiberopsis fossils.

Pyralidae and Choreutidae are both members of the Apoditrysia, a relatively derived clade of ditrysians. Pyraloids, with a fossil record extending to the early Eocene, belong to the diverse clade Obectomera (Kristensen and Skalski, 1999; C. C. Labandeira, personal commun., 2007). The family Pyralidae, however, is a more recent lineage, and extends perhaps to middle Eocene Baltic amber (~44.5 m.y.a.); choreutids lack a fossil record but nevertheless are basal apoditrysians (Kristensen and Skalski, 1999; C. C. Labandeira, personal commun., 2007). Given this, it seems that both the Pyralidae and by phylogenetic relationship, the Choreutidae, could produced the hispine-like damage during the midPaleogene, around the early to middle Eocene, i.e., the more recent “hispine” damage in WiIf et al. (2000). However, based on the current fossil evidence, it is unlikely that these clades could produce the herbivory patterns in the older fossils from late Cretaceous (Kristensen and Skalski, 1999; C. C. Labandeira, personal commun., 2007).

FIGURE 1. Fossil herbivory attributed to an ancestor of extant rolled-leaf beetles (Cephaloleichnites strongi) in Zingiberopsis isonervosa (Zingiberaceae) from early Eocene (1, 3, 5, 8) and extant non-hispine herbivores in five families of Zingiberales (2, 4, 6, 7, 9). 2, Herbivory by Pyralidae (Lepidoptera) in Heliconia imbricata (Heliconiaceae). 4, 9, Herbivory by Pyralidae (Lepidoptera) in Kenealmia alpinia (Zingiberales), a close relative of Zingiberopsis. 6, Herbivory by Anopsilus weevils (Curculionidae) in Canna bangii (Cannaceae). 7, Herbivory by Choreutidae (Lepidoptera) in Calathea crotalifera (Marantaceae). Scale bars in all panels equal 5 mm. (Photos 1, 3, 5, and 8 from Wilf et al., 2000, Science, 289:291-294 with permission from AAAS). Vouchers: (1) (USNM 509718) (J) (USNM 498174) (5) (USNM 498168), (6) (USNM C. Garcia-Robledo 132-135 Anopsilus sp. nov.), (8) (USNM 498169)

TABLE 1-Extant plants from the order Zingiberales and herbivores that produce leaf damage equivalent to that described in fossils of Zingiberopsis. N = number of insects observed in laboratory trials.

The origin of Baridinae (Curculionidae), the subfamily that includes Anopsilus, is not well established (J. Prena, personal commun., 2007). However the earlier fossils of Curculionidae are from the late Cretaceous (Donato et al., 2003). The basal clades of Curculionidae sensu lato are occupied mostly by taxa that feed on monocots, such as Zingiberales (Marvaldi et al., 2002). This suggests that curculionids (and Baridinae, if this is a basal clade of the family) are potential culprits for the oldest Zingiberopsis herbivory.

The ichnotaxon C. strongii predates the oldest known body fossil of this group by ca. 20 My (WiIf et al., 2000). If these feeding tracks were not produced by hispine beetles, this may explain some of the discrepancies between the phylogenies calibrated with this fossil and the phylogenetic analyses based on molecular data alone (Gomez-Zurita et al., 2007). Phylogenies using the fossil herbivory suggest a co-diversification of rolledleaf beetles and its host plants during the Tertiary (McKenna and Farrell, 2006). Phylogenetic analyses based on molecular data alone suggest a more recent origin of rolled-leaf beetles that may radiate later than its host plants (Gomez-Zurita et al., 2007). A potential explanation for the similarity between hispine and non-hispine herbivory patterns is the presence of salt crystals and sclerified vascular bundles in the order Zingiberales (Auerbach and Strong, 1981). These features may predispose both extinct and extant Zingiberales to the convergence of stereotyped epidermal-feeding by different insect taxa (Auerbach and Strong, 1981; Jolivet and Hawkeswood 1995; Garcia-Robledo et al., 2007). In conclusion, it is conceivable that the feeding tracks recorded in Zingiberopsis, as in extant Zingiberales, may belong to insect lineages other than hispines. Therefore, the fossil Cephaloleichnites (Hispinae) must not be solely attributed to an ancestor of the extant rolled-leaf beetles until more conclusive evidence such as the body of a fossil hispine is available.

ACKNOWLEDGMENTS

The Authors want to thank E. K. Kuprewicz for field assistance. Lepidoptera were identified by H. Garcia, Orugas de La Selva Project, Tulane University-Organization for Tropical Studies. J. Prena, USDA Systematic Entomology Laboratory, determined the Anopsilus species as undescribed and shared information on host plants and the phylogenetic relationships of this group with other Curculionidae. Comments by P. Jolivet, E. K. Kuprewicz, C. C. Labandeira, and D. R. Strong improved this paper. This research was supported by the Aldridge Assistantship and the J. McLamore Fellowship, University of Miami and the Organization for Tropical Studies-Donald and Beverly Stone Fellowship to C. Garcia-Robledo.

REFERENCES

AUERBACH, M. J. AND D. R. STRONG. 1981. Nutritional ecology of Heliconia herbivores: Experiments with plant fertilization and alternative hosts. Ecological Monographs, 51:63-83.

DONATO, M., P. POSADAS, D. R. MIRANDA-ESQUIVEL, E. ORTE JAUREGUIZAR, AND G. CLADERA. 2003. Historical biogeography of the Andean region: Evidence from Listroderina (Coleoptera: Curculionidae: Rhytirrhinini) in the context of the South American geobiotic scenario. Biological Journal of the Linnean Society, 80:339-352.

GARCIA-ROBLEDO, C., E. K. KUPREWICZ, AND C. STAINES. 2007. Hispinelike herbivore damage in Canna bangii (Zingiberales, Cannaceae) by Anopsilus weevils (Curculionidae, Baridinae). The Coleopterist Bulletin, 61: 468-470.

GOMEZ-ZURITA, J., T. HUNT, F. KOPLIKU, AND A. P. VOGLER. 2007. Recalibrated tree of leaf beetles (Chrysomelidae) indicates independent diversification of angiosperms and their insect herbivores. PLoS ONE, 4(e360): 1-8.

HICKEY, L. J. AND R. K. PETERSON 1978. Zingiberopsis. A fossil genus of ginger family from late Cretaceous to early Eocene sediments of Western Interior North America. Canadian Journal of Botany, 56:1136-1152.

JOLIVET, P. AND T. J. HAWKESWOOD. 1995. Host plants of Chrysomelidae of the world. An essay about the relationships between the leaf beetles and their food plants. Backhuys Publishers, 281 p.

KRISTENSEN, N. P AND A. W. SKALSKI. 1999. Phylogeny and paleontology, p. 7-25. In N. P Kristensen (ed.), Lepidoptera: Moths and Butterflies. 1. Evolution, Systematics, and Biogeography. Handbook of Zoology, Vol. IV, Pt. 35, De Gruyter, Berlin and New York.

MARVALDI, A., A. SEQUEIRA, C. W. O’BRIEN, AND B. D. FARRELL. 2002. Molecular and morphological phylogenetics of weevils (Coleoptera, Curculionoidea): Do niche shifts accompany diversification? Systematic Biology, 5:761-785.

McCoY, E. D. 1984. Colonization by herbivores of Heliconia spp. plants (Zingiberales: Heliconiaceae). Biotropica, 16:10-13.

MCKENNA, D. D. AND B. D. FARRELL. 2006. Tropical forests are both evolutionary cradles and museums of leaf beetle diversity. Proceedings of the National Academy of Sciences of the United States of America, 103:10947-10951.

STRONG, D. R. 1977. Rolled leaf hispine beetles and their Zingiberales host plants in Middle America. Biotropica, 9:156-169.

WILF, P., C. C. LABANDEIRA, W. J. KRESS, C. L. STAINES, D. M. WINDSOR, A. L. ALLEN, AND K. R. JOHNSON. 2000. Timing the radiations of leaf beetles: Hispines on gingers from latest Cretaceous to recent. Science, 289: 291-294.

ACCEPTED 13 FEBRUARY 2008

CARLOS GARCI;A-ROBLEDO,1 AND CHARLES L. STAINES2

1 Department of Biology, University of Miami, 1301 Memorial Dr., Coral Gables, Florida 33124, ; and @bio.miami.edu>

2 Department of Entomology, National Museum of Natural History, Smithsonian Institution, Washington, D.C. 20560

Copyright Paleontological Society Sep 2008

(c) 2008 Journal of Paleontology. Provided by ProQuest LLC. All rights Reserved.




comments powered by Disqus