Ecological Archives E096-192-A1

María C. Rodríguez-Rodríguez, Pedro Jordano, and Alfredo Valido. 2015. Hotspots of damage by anatgonists shape the spatial structure of plant–pollinator interactions. Ecology 96:2181–2191. http://dx.doi.org/10.1890/14-2467.1

Appendix A. Description of animal mutualists and antagonists included in the study.

The functional group of mutualists includes three animal guilds: bird and lizard legitimate pollinators, as well as facultative bird pollinators. Antagonists are represented by floral herbivores, nectar larcenists, and predispersal seed predators (see Table A1 for species identities).

Mutualists

Pollinators are basically represented by three native species: the Canary Islands chiffchaff Phylloscopuscanariensis (Hartwig, 1886) (Phylloscopidae) and the lacertid Gallotiagalloti (Oudart, 1839) (Lacertidae) as legitimate pollinators, and the African blue tit Cyanistes teneriffae (Lesson, 1831) (Paridae) as facultative bird pollinator that occasionally robs nectar (Fig. A1A-C; Rodríguez-Rodríguez and Valido 2008, Rodríguez-Rodríguez et al. 2013). Birds are more effective pollinators than lizards, primarily due to their higher visitation frequency. However, lizards are comparable to birds in their qualitative pollination effectiveness, especially the adult lizards. Thus, flowers visited only once by a bird or an adult lizard set fruits and viable seeds per fruit in similar proportions (Rodríguez-Rodríguez et al. 2013).

Bird species differ in their foraging behaviors. In contrast to P. canariensis, C. teneriffae occasionally robs nectar making a hole at the corolla base (primary nectar robbery), or simply revisiting previously made holes (secondary nectar robbery) (Fig. A2A). For this, the passerine sometimes tears the corolla to feed on nectar, a destructive behavior also recorded for other native Canarian plants (e.g., Navaea phoenicea (Vent.) Webb & Berthel., González and Fuertes 2011). This mixed mutualistic-antagonistic behavior appears to be not fixed in C. teneriffae. While some individuals always behave as pollinators or nectar robbers, others change from mutualistic to antagonistic foraging even from flower to flower within the same inflorescence. Both adults and juveniles show pure and mixed behaviors (personal observation).

Five more passerine bird species also visit the flowers of Isoplexis canariensis: Sylvia melanocephala (Gmelin, 1789), S. atricapilla (Linnaeus, 1758), S. conspicillata Temminck, 1820(Sylviidae), Fringilla coelebs Linnaeus, 1758, and Serinus canaria (Linnaeus, 1758)(Fringillidae). However, their visitation rate is marginal or practically absent in the study area (Rodríguez-Rodríguez and Valido 2008). All these passerines also act as potential legitimate pollinators except S. canaria, which makes both legitimate and illegitimate floral visits as described for C. teneriffae.

Antagonists

Floral herbivory is caused by Lepidoptera larvae (Fig. A1D). In our study area, we have recorded floral damage by three moth species: the native Gymnoscelis rufifasciata (Haworth, 1809) (Geometridae) and Hypena obsitalis (Hübner, [1813]) (Noctuidae), and the Canarian endemic Choristoneura simonyi (Rebel, 1892) (Tortricidae). Most of observed larvae during fieldwork belonged to G. rufifasciata. This species is distributed in Asia and Europe, including the Canary Islands, and adults may fly throughout the year (Argaman and Wysoki 1991, Báez 1998). This polyphagous moth also feeds on the close continental relatives of Isoplexis species (e.g. Digitalis purpurea L., Petschenka 2010). Although both plant genera are cardenolide rich, this generalist geometrid possibly detoxifies these compounds (Petschenka 2010). Female adults usually oviposit one egg per floral bud in I. canariensis, although eggs may be also present on other inflorescence parts. When feeding on buds, larvae usually ‘enclose’ the flower with silk so they prevent future floral opening and alter its development. The early instar caterpillars feed inside the anthers or the ovary, which are apparently used as protective sites when larvae are very small. As they grow up, larvae leave the reproductive organs and may feed on other floral tissues (e.g., filaments, style, corolla, sepals). Larvae may even move to mature flowers or unripe fruits, causing sometimes the complete loss of gametes and fertilized ovules on an inflorescence (Fig. A2B-E). Fully-grown caterpillars leave inflorescences to continue their development, as we have not seen pupae on the plant. As far as we have observed in the field, caterpillars feed exclusively on I. canariensis flowers, although they eat the leaves in captivity. Apart from Lepidoptera larvae, introduced mammal herbivores (e.g., goats, rabbits) and occasional human gathering (e.g., medicinal properties) also damage the inflorescences. However, both impacts were virtually absent in the study area.

Ants are frequent nectar larcenists during the flowering season, including the native species Plagiolepis barbara Santschi, 1911 and Camponotus hesperius Emery, 1893(Fig. A1E), but also the introduced invader Linepithema humile (Mayr, 1868)(Formicidae). In their search for nectar, ants use holes previously made by nectar-robbing birds or florivorous caterpillars (secondary nectar robbing). They also visit the flower legitimately, but without contacting reproductive organs (nectar theft).

Coleoptera larvae consume developing and mature seeds prior to seed dispersal (probably fam. Kateritidae, Paolo Audisio personal comment; Fig. A1F). One larva is usually found per fruit, and before pupating, they excavate a tunnel later used to exit. Introduced rats (cf. Rattus rattus (Linnaeus, 1758), Muridae) are also predispersal seed predators on developing and ripe fruits. These rodents consume seeds on the infructescence or remove them from the plant, sometimes at further distances. Their damage can be so considerable that would prevent us to estimate the production of fruits and viable seeds in certain plants. This fact, along with their potential role as seed dispersers and introduced status, led us to exclude them from the present study.

Table A1. List of interacting animal species. We indicate their taxonomic status in the Canary Islands (Arechavaleta et al. 2010, Gill and Donsker 2014).

Code: E, Endemic; N, Native; I, Introduced; NA, Not Available.

Fig. A1. Illustrations of the study interacting animals. Mutualists: (A) Phylloscopus canariensis, (B) Cyanistes teneriffae, (C) Gallotia galloti. Antagonists: (D) larvae of Gymnoscelis rufifasciata, (E) Camponotus hesperius, (F) Coleoptera larvae (cf. fam. Kateritidae). Photo credits: M. C. Rodríguez-Rodríguez (A, D–F), P. Felipe (B–C).

Fig. A2. Floral damage by the occasional nectar robber Cyanistes teneriffae (A) and floral herbivores (B-E) in different stages of floral development. Photo credits: M. C. Rodríguez-Rodríguez.

Literature cited

Arechavaleta, M., S. Rodríguez, N. Zurita and A. García. 2010. Lista de especies silvestres de Canarias. Hongos, plantas y animales terrestres. Gobierno de Canarias, Santa Cruz de Tenerife.

Argaman, Q., and M. Wysoki. 1991. The flower-eating Gymnoscelis (Lep. Geometridae) in Israel. Tropical Pest Management 37:185–187.

Báez, M. 1998. Mariposas de Canarias. Editorial Rueda, S.L., Madrid.

Gill, F., and D. Donsker. 2014. IOC World Bird List (v 4. 4).

González, A, and J. Fuertes. 2011. Ecología y evolución de las plantas ornitófilas de la Macaronesia. El Indiferente 21: 4–75.

Petschenka, G. 2010. Physiological adaptations of specialized insects to host plant cardenolides. Dissertation. University of Hamburg.

Rodríguez-Rodríguez, M. C., and A. Valido. 2008. Opportunistic nectar-feeding birds are effective pollinators of bird-flowers from Canary Islands: experimental evidence from Isoplexis canariensis (Scrophulariaceae). American Journal of Botany 95:1408–1415.

Rodríguez-Rodríguez, M. C., P. Jordano, and A. Valido. 013. Quantity and quality components of effectiveness in insular pollinator assemblages. Oecologia 173:179–190.

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