Interciencia ISSN: 0378-1844 [email protected] Asociación Interciencia Venezuela Pelayo, Roxibell C.; Rengifo, Carlos; Soriano, Pascual J. Avian nectar robbers of Passiflora mixta (Passifloraceae): do they have a positive effect on the plant? Interciencia, vol. 36, núm. 8, agosto, 2011, pp. 587-592 Asociación Interciencia Caracas, Venezuela Available in: http://www.redalyc.org/articulo.oa?id=33921395005 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative AVIAN NECTAR ROBBERS OF Passiflora mixta (Passifloraceae): DO thEY havE A POSitivE EffEct ON thE PLant? ROXibELL C. PELAYO, CARLOS RENGifO and PASCUAL J. SORianO SUMMARY The effect of nectar robbing on plant reproduction may be found associated with P. mixta flowers: five hummingbirds, negative, positive or neutral. The effect was evaluated on Pas- two flower-piercers and one oriole. Experiments support the siflora mixta, an Andean high-mountain species that is pol- plant self-incompatibility. Nectar robbers do not harm the linated by the Sword-billed Hummingbird (Ensifera ensifera). plant reproductive structure. The effect of nectar robbing ap- We determined: 1) the bird assemblage associated with P. mix- pears to be positive, since robbers diminish the resource of- ta flowers, 2) the P. mixta flower nectar production pattern, fered increasing pollen flow. In consequence, the effect of 3) how nectar robbing affects fruit and seed production and nectar robbers on P. mixta could be considered a relation of 4) self-incompatibility in this species. Eight bird species were indirect mutualism lant-pollinator interac- mate pollinator (Irwin and Brody, 1998; It is known that nectar tions may be affected by Maloof and Inouye, 2000). Nectar robbers robbing can be positive, negative or neu- animals that exhibit a may not always exhibit this behavior if tral, and can exert a selection pressure on type of behavior called cheating; that is, they are able to act as legitimate visitors flower morphology and plant-pollinator in- they obtain the reward involved in a mutu- to the flowers of other plant species. How- teractions (Arizmendi et al., 1996; Trave- alistic interaction without providing the ever, they show a preference for flowers set et al., 1998; Maloof and Inouye, 2000; corresponding pollination service (Tyre with corollas that are long and/or produce Irwin et al., 2001; Lara and Ornelas, 2001; and Addicott, 1993; Addicott and Tyre, large amounts of nectar (Maloof and In- Navarro, 2001; Kjonaas and Rengifo, 1995; Morris, 1996). Examples of this be- ouye, 2000; Lara and Ornelas, 2001). 2006). In the majority of papers indicating havior are the so called nectar robbers, Sword-billed Humming- that nectar robbing diminishes the plant`s which can be a bird, an insect or another bird usually act as nectar robbers on flowers fitness; the effective pollinator is a hum- animal capable of extracting nectar from with long corollas, while all the species of mingbird, which suggests that the systems flowers through an opening made in the the genera Diglossa and Diglossopis (Thrau- mentioned could be the most susceptible base of the corolla. This type of illegiti- pidae), so-called flower-piercers, exhibit this ones to affected by this phenomenon. mate visit is classified as primary, if they behavior. Some Psittacidae, Fringillidae and The passion flower Pas- perforate the corolla, and secondary, if other Thraupidae also engage in this behav- siflora mixta L. (Passifloraceae) is dis- they take advantage of holes made by oth- ior (Lyon and Chadek, 1971; Graves, 1982; tributed from Venezuela to Bolivia, from er robbers (Inouye, 1980; Irwin, 2000; Roubik et al., 1985; Arizmendi et al., 1996; 1700 to 3700masl. Its exclusive pollina- Maloof and Inouye, 2000). Additionally, Traveset et al., 1998; Isler and Isler, 1999; tor is the Sword-billed Hummingbird this type of interaction can affect the Cotton, 2001; Lara and Ornelas, 2001; Na- (Ensifera ensifera Boissoneau), which is abundance of nectar available to the legiti- varro, 2001). the only species that makes legitimate KEYWORDS / Andes / Ensifera ensifera / Hummingbird / Nectar Robbers / Venezuela / Received: 06/05/2010. Modified: 05/06/2011. Accepted: 05/08/2011. Roxibell C. Pelayo. Biologist and M.Sc. in Tropical Ecology, Instituto de Ciencias Ambientales y Ecológicas (ICAE), Universidad de Los Andes (ULA), Venezuela. Professor, ULA, Venezuela. e-mail: [email protected] Carlos Rengifo. Biologist and M.Sc. in Tropical Ecology, ICAE-ULA, Venezuela. Director, Or- nithological Station La Mucuy, Nacional Park Sierra Nevada, Mérida, Venezuela. Pascual J. Soriano. Biologist, M.Sc. and Doctor in Tropical Ecology, ICAE-ULA, Venezuela. Professor, ULA, Venezuela. AUG 2011, VOL. 36 Nº 8 0378-1844/11/08/587-06 $ 3.00/0 587 587 PELAYO 6.indd 587 04/08/2011 18:56:22 visits to its flowers (Escobar, 1988; Ensifera ensifera on the flowers used for measurements Lindberg and Olesen, 2001). The two (n=14), part of the hypanthium was covered species have a similar geographical dis- The Sword-billed Hum- with acetate rings, including the area where tribution suggesting a co-evolutionary mingbird E. ensifera is a traplinner species the nectary is found internally, and each process (Snow and Snow, 1980; Lindberg weighing 12g and has a body length of flower was isolated in a veil bag. and Olesen, 2001). 140mm. It has an unusually long bill Analysis of variance for We deem important to (102mm males, 114mm females) bent slight- repeated measurements on the volume and evaluate the effect of nectar robbing on ly upwards (Garrison and Gass, 1999; concentration data was performed (p<0.05) P. mixta, a plant that belongs to a polli- G u t i é r r e z et al., 2004a, b; Hilty, 2003). in order to determine differences among nator system restricted to the high Ande- the anthesis days and/or among the flowers an mountains, involving a hummingbird Assemblage of birds associated with P. measured. Additionally, in order to test if species as the effective pollinator and mixta flowers avian visits were associated with volume or could be negatively affected by nectar nectar concentration, Spearman correlations robbing. Hence, the general objective was Along the border of the between the average nectar volumes pro- to study the effect of nectar robbing on Motatán River, 12 patches 1 to 50m2 of P. duced on the second day, the third day and the plant-pollinator interaction and P. mixta were selected, physically separated the average for both days, and the activity mixta fitness. Specific objectives included: from 10 to 200m. Between March-June patterns of each bird species were carried 1) to determine the bird assemblage asso- 2005 and March-April 2006, the avian visi- out. In these analyses, the first day of an- ciated with P. mixta flowers, 2) to deter- tors (36-175 flowers), were recorded using thesis was not considered because nectar mine the P. mixta flower nectar produc- binoculars (10×40) during 1h observation production was very low during that day. tion pattern, 3) to evaluate how nectar cycles (0630-1900h) for a total observation robbing affects fruit and seed production, time of 120h. As the number of flowers Reproductive biology and 4) to evaluate self-incompatibility in varied according to time and site, the total this plant species. effort was 12750h/flower. Bird species were Between September 2005 identified using the Venezuelan bird guide and January 2006 the breeding system of Methods (Hilty, 2003) and the type of visit (legiti- the flowers was determined through a field mate or nectar robbing) was recorded. Nec- experiment consisting of three treatments: Study site tar robbing species were classified as pri- 1) Autogamy (n=16): un-opened flowers mary robbers and secondary robbers. Like- were selected and covered with veil bags Fieldwork was carried wise, for each species, the cumulative visit that prevented the access of any visitor. Si- out in El Rincón de la Venta, a locality frequency was calculated, standardizing the multaneously, the flowers were fertilized in the middle basin of the Motatán River, data for 1000 flowers per time interval. The manually, with their own pollen, as they 10km south-west of Timotes, Mérida variation throughout the day. The Esti- are herkogamics (anthers are 8-10mm be- State, Venezuela (8°54'38''N, mateS program was used to generate rar- low the stigma). 70°46'46''W), at an altitude of 2900m. efaction curves with the Mao Tao indices The site occupies a dry slope on the lim- and the Chao 2 and Jackknife 1 richness 2) Xenogamy (n=9): un-opened flowers its between the Andean páramo and indices (Colwell, 2005) were calculated. Fi- were emasculated before the anthers high-mountain dry evergreen forest eco- nally, we determined the differences of the reached maturity. Manual pollination was logical units (Ataroff and Sarmiento, bird species visit frequency by means of a performed with pollen from different and 2003). Temperature follows an isothermal chi-square and standardized residuals test spatially distant (>20-50m) individuals. pattern with a yearly average of 10.2°C, (Zar, 1999). 3) Controls (n=14): flowers exposed to pol- while annual precipitation averages linator visits. 1065mm, with a bimodal distribution and Nectar production pattern: volume- peaks in February and June. The site ex- concentration All three treatments were hibits a significant degree of anthropic al- carried out simultaneously on flowers be- teration produced by the expansion of the Volume and concentration longing to the same patch. For manual fer- agricultural frontier, where, besides Pas- of the nectar produced during the period tilization, an artist’s paintbrush was used siflora mixta, species of the Espeletia, between anthesis and wilting (3 days) was and washed with distilled water after each Baccharis, Vaccinium, Echeveria, Lupi- calculated for each flower.