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

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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.

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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. For this purpose, pollen application. Pollination was per- nus, Psammisia and Fuchsia genera pre- a hole was made in the base of the hypan- formed twice a day (morning and after- dominate. thium using a 100µl capillary tube; imme- noon) from the day of anthesis until the diately thereafter, as many as 20µl capillary flowers wilted. Stigmatic receptivity tests in Passiflora mixta tubes as necessary to extract all the nectar different flowers (n=57) were carried out by found in the nectar chamber were intro- determining peroxidase enzyme activity, P. mixta is a climbing duced, measuring the length of the nectar submerging the stigmas in 3% hydrogen and long-lived perennial plant, with angular column in the capillary tubes to determine peroxide at different times of the day in the striated stems and trilobulate leaves with the volume. This procedure was repeated at three anthesis days (Kearns and Inouye, serrated borders. Flowers are long tubular 1h intervals between 06:30 and 18:30. Us- 1993); these flowers were not used in the (135mm), erect or horizontal, with cylindri- ing a field refractometer (Eclipse, Belling­ breeding system experiments. cal green hypanthia that turn pink toward ham+Stan­ley), the sugar concentration in All the flowers were pro- the apex, pink/yellow colored sepals; petals each of the samples was determined. In or- tected from nectar robbing by placing ace- subequal to the sepals, corona in a series, der to obtain the nectar production patterns tate rings over the nectary. Each of the usually purple. It flowers and yields fruit from each flower, the same flowers were flowers in the three treatments were labeled throughout the year, and it has been sug- measured from the time that they opened with colored tape, placed under the stipules gested that it is self-incompatible (Escobar, until they closed. To prevent robbing and of the pedicel base, so that the abscission 1988; Lindberg and Olesen, 2001). legitimate visits before and during anthesis scar could be detected in case of abortion.

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587 PELAYO 6.indd 588 04/08/2011 18:56:23 In all cases, the flowers were moni- Table I E. ensifera. As far as E. ensifera tored until fruit production and the Bird species associated with is concerned, it never showed number of seeds in each one was Passiflora mixta flowers aggressive behavior nor was it counted. Species NR1 NR2 LV displaced by any other bird spe- Two circumstanc- cies. es significantly limited the number Heliangelus mavors (Trochilidae) + + - All the short-billed hum- of replicates in the three treat- Metallura tyrianthina (Trochilidae) - + - mingbird species that acted as ments: the low number of open Coeligena eos (Trochilidae) - + - nectar robbers on P. mixta visit- flowers on their first day of anthe- Colibri coruscans (Trochilidae) - + - ed legitimately the flowers of sis, so as to conduct all the treat- Diglossa gloriosa (Thraupidae) + + - Fuchsia spp. (Onagraceae), ments simultaneously, and the fact Diglossa sittoides (Thraupidae) + + - Psammissia sp. (Ericaceae) and that a high number of the used Icterus chrysater (Icteridae) + - - Salvia sp. (Lamiaceae). Insects flowers were destroyed by slugs. Ensifera ensifera (Trochilidae) - - + were also observed in associa- NR1: primary nectar robbers, NR2: secondary nectar robbers, LV: tion with P. mixta flowers, the Effect of nectar robbing on legitimate visitor. The + and - signs indicate, respectively, that the most conspicuous being bumble- reproductive activity of the plant bird exhibits positive or negative behavior for the type of interaction bees that act as primary robbers, taken into consideration. beetles as secondary robbers The procedure and pollen consumers, as well for measuring and comparing fruit and as bees that robbed nectar. seed production during low and high flores- E. ensifera showed two cence intervals was as follows. From Sep- Results activity peaks, one in the morning and the tember-December 2005 (low florescence in- other in the afternoon; however, the most terval; 0-35 flowers) 31 robbed and 31 un- Avian assemblage and other animals frequent robbers (D. gloriosa and H. ma- robbed flowers were selected, and from associated with P. mixta vors) made significant use of the resource March-September 2006 (high florescence throughout the day. On the other hand, M. interval; 4-180 flowers) 45 robbed and 56 Eight bird species were tyrianthina showed a visiting behavior sim- unrobbed flowers were selected, all belong- found associated with P. mixta flowers (Ta- ilar to that of E. ensifera, while the rest of ing to the same patches used during the ob- ble I). Hemispingus superciliaris (Thraupi- the nectar robbers showed no clear visiting servations of avian flower visitors. Exclud- dae) was also recorded at the study site pattern (Figure 2). According to the chi- 2 ers (acetate rings on the base of the hypan- outside the observation periods, as well as square test (χ 8= 4203, p>0.005), the per- thium) were placed on the unrobbed flow- Heliangelus spencei and Diglossa albilatera centage of illegitimate visits (85%) was sig- ers to prevent nectar robbing while near the study site. The species accumula- nificantly greater than that of legitimate permitting legitimate flower visits. Robbed tion curve reached saturation with eight ones (15%). As far as standardized residu- flowers were not manipulated. Finally, fruit species; however, the rarefaction model pre- als are concerned, they proved that such seed sets were counted. dicted the possibility of a pair of additional differences are determined mainly by the species (Figure 1). Likewise, the Chao 2 visiting frequency of H. mavors, M. tyrian- Damage to floral structures by nectar and Jackknife 1 richness indices estimated thina, C. eos, E. ensifera and D. gloriosa. robbers a number of species slightly greater than found (8.49 and 9.96, respectively). Never- Nectar production pattern: volume and In order to determine theless, our empirical data are located on concentration whether the robbers caused any damage to the lower limit of the Chao 2 richness esti- the reproductive organs (ovaries, stigmas, mator confidence interval (Figure 1). The measured flowers anthers or androgynophore), 54 robbed Of all the species recorded, E. en- showed different production patterns, with flowers were randomly selected to compare sifera was the only one that always made asynchronous peaks. However, upon aver- their reproductive structures with those that legitimate visits, while the rest of the visi- aging the daily values, some regularity was remained intact (n=20). tors were nectar robbers. Only D. gloriosa, found. On the first day, nectar production D. sittoides, H. superciliaris, I. took place only toward the end of the after- chrysater, and rarely H. mavors noon and volumes were very low (average were primary robbers, while the of 5.1µl; SD= 0.83; n= 14). On the second rest of the hummingbirds did so day, the average was 182µl (SD= 8.24; n= as secondary robbers. When the 14), being the largest production compared flower had been previously per- with all other days, and production was er- forated, D. gloriosa and H. ma- ratic (Figure 3). On the third day, nectar vors acted as secondary robbers. volume decreased (average= 39.66µl; SD= No nectar robbers were observed 6.7; n= 14), a peak being observed only in coming into contact with flower the morning. Nectar volume varied signifi- reproductive structures. cantly on the three days of anthesis (F1.13= Diglossa gloriosa and H. 18.8; p<0.0001), but not among the flowers mavors exhibited territorial be- (F1.13= 1.72; P= 0.05). havior, aggressively defending On the first day of anthe- the patches from their own and sis, concentration tended to increase slightly other species. Diglossa gloriosa in the late afternoon. On the second day, Figure 1. Accumulation curves (solid line) and rarefaction displaced H. mavors and other lower values were recorded early in the (dashed line) for birds associated with Passiflora mixta hummingbirds, while H. mavors morning and at the end of the afternoon, flowers and their confidence interval (dotted lines). Mao did so with the rest of the hum- while the pattern on the third day was very Tao index. mingbirds, with the exception of similar to that of the second day, except

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587 PELAYO 6.indd 589 04/08/2011 18:56:23 that during the early morning nectar robbing, they produced hours, values were not quite as an average of 149 ±68.7 seeds high (Figure 3). On the third per fruit. day, nectar volume decreased (average= 39.7 ±6.7µl), a peak Damage to the floral structures being observed only in the during the nectar robbing morning. Nectar concentration process averaged 23.03 ±2.66% and showed no significant differenc- No visible differences es among the days (F1.13= 0.22; in the reproductive structures P= 0.64), but it did among flow- of robbed and unrobbed flow- ers, fluctuating between 2 and ers were detected. Hence, the 36.5% (F1.13= 17.58; p<0.0001). nectar robbers apparently lim- These flowers open at night. ited themselves to piercing The mean volume pro- holes only in the wall of the duced by day and the average hypanthium, without harming of the second and third days anthers, stigmas, ovaries or showed no significant correla- androgynophore. Two types of tion with bird activity patterns, scars were identified: one of except for four cases in which a Figure 2. Frequency of visits throughout the day by bird species associ- them made by flower piercers very low correlation was found: ated with Passiflora mixta. (76%), which consisted of two the first on day one with C. eos holes, one circular and one (r= 0.65) and three on day two that in- in order to evaluate whether they showed elongated, corresponding to the penetra- volved M. tyrianthina (r= 0.64), D. gloriosa evidence of having suffered nectar robbing, tion of the hypanthium by the lower and (r= 0.67) and I. chrysater (r= 0.62). and calculated the average of the seeds pro- upper part of the bill, respectively; the duced per fruit. Although 100% of the other corresponds to bumblebees (24%), Reproductive biology fruits showed evidence of having suffered with holes and sizes of various shapes, since these animals chew the In the autogamy treat- surface of the nectary. Scars of ments and their control, 100% of both types were located on the the flowers aborted, while in the part of the hypanthium covering xenogamy treatment, 78.8% did the nectary at an average of so; that is, two out of nine flow- 6.6mm (SD= 0.26; n= 28) from ers taken into consideration pro- the base of the hypanthium. In- duced fruits. Seed production spection of the flowers showed was 137 and 139 seeds per fruit that 77% of them had suffered in the two treatments. The stig- nectar robbing. matic receptivity tests (n= 45) were positive in 100% of cases. Discussion

Effect of nectar robbing on the In spite of the bird assem- reproductive activity of the plant blage being located on the lower limit predicted by the Chao 2 Of the flowers marked richness estimator, the value ob- during the low florescence in- tained is a good approximation of terval (September-December reality, since the cause of the 2005) that had suffered nectar large confidence intervals in the robbing, 100% aborted, while estimator was the presence of I. 96.9% of the protected flowers chrysater and C. coruscans, spe- did the same, which represents cies that are infrequent at the that one of the 31 observed site; I. chrysater is found on the flowers fructified and produced upper limit of its altitudinal dis- 117 seeds. In the experiments tribution, while C. coruscans mi- carried out during the flores- grates between the cloud forest cence peak (March-September and páramo ecological units 2006), 38% of the robbed flow- (Hilty, 2003; Rengifo et al., ers and 96% of the unrobed 2005). In addition, these two spe- ones aborted. These results are cies could be classified as occa- contrary to expectation. Aver- sional visitors since their fre- age seed production was 151 ±7 quency is considerably lower than and 81 ±16, respectively. other bird species. As far as I. In view of the high per- chrysater is concerned, this is centage of abortions among the the first record of an Icteridae as flowers used in September 2005, Figure 3. Sugar volume and concentration of nectar produced by Pas- a nectar robber, notwithstanding 21 fruits were randomly collect- siflora mixta flowers (n= 14) during anthesis days. The bars represent that the greater interrelation of ed from the patches employed, the standard deviation for each point on the graphs. this species with the plant must

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587 PELAYO 6.indd 590 04/08/2011 18:56:24 be with its fruits. For this reason, together tively intermittent throughout the day and support and assistance during field work, with T. fuscater, it should be considered as that these flowers are also robbed could be Jesús Lobo and Rafael Colmenares for al- a potential seed disperser. E. ensifera is interpreted as a special case of bonanza- lowing to carry out experiments on their the only species exhibiting morphological blank pattern (Feinsinger, 1978, 1983). Ad- land, and Pedro Jiménez, Javier Estrada, correspondence with P. mixta flowers, ditionally, our data support the existence Daniel Larrea, Adriana Ruiz and Richard which allows it to make legitimate visits of self-incompatibility in P. mixta since, in Smith for their valuable comments. Miguel (Table I). In spite of this, the nectar of- spite of its low values, the xenogamy Molinari made the taxonomic identification fered by these flowers was consumed by a treatment was the only one where pollina- of the plants. The work was financed par- significant number of nectarivorous species tion was successful, which proves the im- tially by CDCHT-ULA (Project C‑1339-05- that, not having the anatomical attributes portance of cross-fertilization in the repro- 01-F) and IDEA WILD. that allow them to visit the flowers fron- ductive success of the plants. Likewise, we tally, make illegitimate visits, acting as interpret the abortion of all the flowers in REFERENCES nectar robbers. Additionally, the extraordi- the control treatment as another indication nary length of the androgynophore (9.7 of self-incompatibility since it was evident Addicott JF, Tyre AJ (1995) Cheating in an obli- ±4.45mm) does not allow an accidental that during the experiment, that took place gate mutualism: how often do yucca moths benefit yuccas? Oikos 72: 382-394. contact of any part of the bodies of these out of the flowering peak, E. ensifera did animals with anthers or with stigmas, Arizmendi MC, Domínguez CA, Dirzo R (1996) not show the expected visit frequency. The role of avian nectar robber and of hum- thereby preventing them from acting as The finding that 100% of mingbird pollinators in the reproduction of accidental pollinators. the fruits collected in the field showed evi- two plant species. Funct. Ecol. 10: 119-127. The foraging patterns of dence of having been robbed suggests that Ataroff M, Sarmiento L (2003) Diversidad en Los nectar robbers confirm the importance of the effect cannot be negative. On the con- Andes de Venezuela. I. Mapa de Unidades this resource in their diet, since all of trary, evidence indicates a possible posi- Ecológicas del Estado Mérida. Ediciones Insti- them showed high visit frequency through- tive effect: 1) during the peak flowering tuto de Ciencias Ambientales y Ecológicas (ICAE), Universidad de Los Andes, Mérida, out the day. Moreover, activities of M. tyr- period a greater number of aborted flowers Venezuela. CD-ROM. ianthina, C. eos and D. gloriosa were pos- was found among the unrobbed than the Colwell RK (1995) Effects of nectar consumption itively correlated with the nectar produc- robbed ones, and 2) the robbed flowers by the hummingbird flower mite Proctolaelaps tion pattern. In spite of the lack of correla- produced a greater average number of kirmsei on nectar availability in Hamelia pat- tion between E. ensifera activity and seeds than unrobbed flowers. A possible ens. Biotropica 27: 206-217. nectar production, it shows two well de- explanation for this phenomenon is that if Colwell RK (2005) EstimateS: Statistical Estima- fined peaks during the times of day when the nectar robbers diminish the resource tion of Species Richness and Shared Species the energy demand is greater, that is, at available for the pollinator that must visit from Samples. Version 7.5. Persistent URL. the beginning of the morning and at the more flowers per time unit (Zimmerman Cotton PA (2001) The behavior and interactions of birds visiting Erythrina fusca flowers in the end of the afternoon (Gass and Garrison, and Cook, 1985), consequently increment- Colombian Amazon. Biotropica 33: 662-669. 1999). This supports the importance of P. ing pollen flow in the population, could be Escobar LK (1988) Passifloraceae monografía . 10 mixta in the energy budget of E. ensifera. an adaptive advantage for this self-incom- Flora de Colombia. Instituto de Ciencias Natu- The data obtained also shows that flower patible plant. Several studies have shown rales, Museo de Ciencia Natural, Universidad piercers are the most important robbers of that higher floral visit frequency and lon- Nacional de Colombia. Bogotá. Clombia. these flowers, both because of the high ger visits lead to increased fruit and seed Feinsinger P (1978) Ecological interactions be- visiting frequency and because they are set (Thomson and Plowright, 1980; Feins- tween plants and hummingbirds in a succes- mainly the ones that perforate and expose inger, 1983; Lanza et al., 1995; Husband sional tropical community. Ecol. Monogr. 48: 269-287. them to other avian visitors. All the holes and Schemske, 1996). Moreover, since the made by the nectar robbers are found only Feinsinger P (1983) Variable nectar secretion in a pollinator is a trapliner species with high Heliconia species pollinated by hermit hum- on the surface that is occupied internally energy demands that must be satisfied by mingbirds. Biotropica 15: 48-52. by the nectary. a mutualistic species that, like P. mixta, Garrison SE, Gass CL (1999) Response of a tra- The nectar production offers considerable nectar volume and con- plining hummingbird to changes in nectar pattern of P. mixta is very similar to that centration, the absence of robbers would availability. Behav. Ecol. 10: 714-725. of other high mountain species with anthe- allow the requirements of E. ensifera to be Gass CL, Garrison SE (1999) Energy regulation by sis lasting more than 1 day, with the larg- satisfied with fewer visits, thus reducing traplining hummingbirds. Funct. Ecol. 13: er volumes produced about mid-anthesis, pollen flow and with it the probability of 483-492. and constant sugar concentration during cross-pollination success. Graves GR (1982) Pollination of a Tristerix mistle- all the days (Navarro, 2001). However, the In summary, in this toe (Loranthaceae) by Diglossa (Ave, Thraupi- dae). Biotropica 14: 316-317. present values of nectar volume and sugar study the reproductive success of P. mixta concentration are greater than those re- Gutiérrez-Z A, Carrillo E, Rojas S (2004a) Guía was determined mainly by the presence of Ilustrada de los Colibríes de la Reserva Natu- ported for other ornithophilous flowers, its pollinator (E. ensifera) during the flow- ral Río Ñambí. FPAA, FELCA, ECOTONO. both from high mountain and low land ering peak months. Simultaneously, this Bogotá, Colombia. 156 pp. (Waser, 1979; Willmer and Corbet, 1981; success was favored by the visits of nectar Gutiérrez-Z A, Rojas-Nossa S, Stiles G (2004b) Roubik et al., 1985; Colwell, 1995; Ariz- robbers, which diminished the resource of- Dinámica poblacional de la interacción colibrí- mendi et al., 1996; Lange et al., 2000; Na- fered per flower and could be inducing an flor en ecosistemas altoandinos. Ornitol. Neo- varro, 2001). increase in pollen flow. Therefore, nectar trop. 15: 205-213. Finding an erratic nectar robbers could be considered as an indirect Hilty SL (2003) Birds of Venezuela. 2nd ed. Princ- eton University Press. Princeton, NJ, USA. production pattern on a populational level mutualistic species of P. mixta. 876 pp. implies that nectar is available for the Husband BC, Schemske DW (1996) Evolution of birds throughout the day, which explains ACKNOWLEDGEMENTS the magnitude and timing of inbreeding de- that the most frequent nectar robbers show pression in plants. Evolution 50: 54-70. high visiting rates all day long. The fact The authors thank Teresa Inouye DW (1980) The terminology of floral larce- that nectar production per flower is rela- Schwarzkopf and Ilba López for logistical ny. Ecology 61: 1251-1252.

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587 PELAYO 6.indd 591 04/08/2011 18:56:24 Irwin RE (2000) Hummingbird avoidance of nec- of Impatiens capensis at the individual, Snow DW, Snow BK (1980) Relationship between tar-robbed plants: spatial location or visual plant, and population levels. Oecologia 102: hummingbirds and flowers in the Andes of cues. Oikos 91: 499-506. 113-119. Colombia. Bull. Br. Mus. Nat. Hist. (Zool.) 38: Irwin RE, Brody AK (1998) Nectar robbing in Ipo- Lindberg AB, Olesen JM (2001) The fragility of 105-139. mopsis aggregata: effects on pollinator behav- extreme specialization: Passiflora mixta and its Thomson JD, Plowright RC (1980) Pollen carryo- ior and plant fitness. Oecologia 116: 519-527. pollinating hummingbird Ensifera ensifera. J. ver, nectar rewards, and pollinator behavior Irwin RE, Brody AK, Waser NM (2001) The im- Trop. Ecol. 17: 323-329. with special reference to Diervilla conicera. pact of floral larceny on individuals, popula- Lyon DL, Chadek C (1971) Exploitation of nectar Oecologia 46: 68-74. tions and communities. Oecologia 129:161-168. resources by hummingbirds, bees (Bombus) Traveset A, Willson MF, Sabag C (1998) Effects of Isler ML, Isler PR (1999) Tanagers: Natural Histo- and Diglossa baritula and its role in the nectar-robbing birds on fruit set of Fuchsia ry, Distribution and Identification. Smithson- evolution of Penstemon kunthii. Condor 73: magellanica in Tierra del Fuego: a disrupted ian Institution Press. Washington, DC, USA. 246-248. mutualism. Funct. Ecol. 12: 459-464. 406 pp. Maloof JE, Inouye DW (2000) Are nectar robbers Tyre AJ, Addicott JF (1993) Facultative non-mutu- Kearns CA, Inouye DW (1993) Techniques for Pol- cheaters or mutualists? Ecology 81: 2651-2661. alistic behaviour by an “obligate” mutualist: lination Biologists. University Press of Colora- Morris WF (1996) Mutualism denied? Nectar-rob- “cheating” by yucca moths. Oecologia 94: 173-175. do. Niwot, CO, USA. 583 pp. bing bumblebees do not reduce female or male Kjonaas C, Rengifo C (2006) Differential effects of success of bluebells. Ecology 77: 1451-1462. Waser NM (1979) Pollinator availability as a deter- minant of flowering time in ocotilo Fouquie ( - avian nectar robbing on fruit set of two Vene- Navarro L (2001) Reproductive biology and effect ria splendens). Oecologia 39: 107-121. zuelan Andean cloud forest plants. Biotropica of nectar robbing on fruit production in Ma- 38: 1-4. cleania bullata (Ericaceae). Plant Ecol. 152: Willmer PG, Corbet SA (1981) Temporal and mi- Lara C, Ornelas JF (2001) Preferential nectar rob- 59-65. croclimatic partitioning of the floral resources of Justicia aurea amongst a concourse of pol- bing of flowers with long corollas: experimental Rengifo C, Nava A, Zambrano M (2005) Lista de len vectors and nectar robbers. Oecologia 51: studies of two hummingbird species visiting Aves de La Mucuy y Mucubají. Parque Nacio- 67-78. three plant species. Oecologia 128: 263-273. nal Sierra Nevada, Mérida-Venezuela. Serie Lange RS, Scobell SA, Scott PE (2000) Humming- Aves de Mérida. Vol. 1. Editorial Venezolana. Zar JH (1999) Biostatistical Analysis. 4th ed. Prentice bird-syndrome traits, breeding system and pol- Mérida, Venezuela. Hall. Upper Saddle River, NJ, USA. 663 pp. lination effectiveness in two syntopic Penste- Roubik DW, Holdbrook NM, Parra G (1985) Roles Zimmerman M, Cook S (1985) Pollinator foraging, mon species. Int. J. Plant Sci. 161: 253-263. of nectar robbers in reproduction of the tropi- experimental nectar-robbing and plant fitness Lanza Z, Smith GC, Sack S, Cash A (1995) cal treelet Quassia amara (Simaroubaceae). in Impatiens capensis. Am. Midland Nat. 143: Variation in nectar volume and composition Oecologia 66: 161-167. 84-90.

AVES LADRONAS DE NÉCTAR DE Passiflora mixta (Passifloraceae) ¿TIENEN EFECTO POSITIVO EN LA PLANTA? Roxibell C. Pelayo, Carlos Rengifo y Pascual J. Soriano RESUMEN

El efecto del robo de néctar sobre la reproducción de plantas de P. mixta: cinco colibríes, dos diglosas y un icterido. Los experi- puede ser negativo, positivo o neutro. Se evaluó su efecto en Pas- mentos apoyan la auto-incompatibilidad de la planta. Los ladrones siflora mixta, una planta de la alta montaña andina que es poli- de néctar no dañan las estructuras reproductivas de las flores. Se nizada por el colibrí pico de espada (Ensifera ensifera). Se deter- concluye que en este sistema el efecto del robo de néctar podría minó (1) el ensamble de aves asociados a las flores de P. mixta, ser positivo; pues los ladrones al disminuir el néctar ofrecido por (2) el patrón de producción de néctar de las flores de P. mixta, las flores, inducirían un aumento en el flujo de polen. En conse- (3) cómo el robo de néctar afecta la producción de frutos y se- cuencia, la establecida entre P. mixta y sus ladrones de néctar millas, y (4) la auto-incompatibilidad en las flores de esta especie. puede ser considerada como una relación indirecta mutualista. Encontramos que ocho especies de aves se asocian con las flores

AVES LADRAS DE NÉCTAR DE Passiflora mixta (Passifloraceae) TÊM EFEITO POSITIVO NA PLANTA? Roxibell C. Pelayo, Carlos Rengifo e Pascual J. Soriano RESUMO

O efeito do roubo de néctar na reprodução das plantas pode de P. mixta: cinco beija-flores, dois picaflores e um corrupião. ser negativo, positivo ou neutro. Tal efeito foi avaliado em Pas- Os experimentos apoiam a autoincompatibilidade da planta. siflora mixta, espécie de altas montanhas andinas que é poli- Os ladrões de néctar não danificam a estrutura reprodutiva da nizada pelo beija-flor-bico-de-espada (Ensifera ensifera). De- planta. O efeito do roubo de néctar parece ser positivo, já que terminaram-se: 1) o conjunto de pássaros associados às flores os ladrões diminuem o recurso oferecido, incrementando o flu- de P. mixta, 2) o padrão de produção do néctar de P. mixta, xo de pólen. Em consequência, o efeito dos ladrões de néctar 3) a maneira em que o roubo de néctar afeta a produção de em P. mista poderia ser considerado como uma relação de mu- frutos e sementes, e 4) a autoincompatibilidade nesta espécie. tualismo indireto. Encontraram-se oito espécies de pássaros associadas a flores

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