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Nectar Removal Effects on Seed Production in Moussonia Deppeana (Gesneriaceae), a Hummingbird-Pollinated Shrub1

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Nectar Removal Effects on Seed Production in Moussonia Deppeana (Gesneriaceae), a Hummingbird-Pollinated Shrub1 14 (1): 117-123 (2007) Nectar removal effects on seed production in Moussonia deppeana (Gesneriaceae), a hummingbird-pollinated shrub1 Juan Francisco ORNELAS & Mariano ORDANO, Departamento de Biología Evolutiva, Instituto de Ecología, A.C., Km 2.5 Carretera Antigua a Coatepec No. 351, Congregación El Haya, Apdo. Postal 63, Xalapa, Veracruz 91070, México. Carlos LARA2, Laboratorio de Ecología de la Conducta, Centro Tlaxcala de Biología de la Conducta, UAT–UNAM, Km 1.5 carretera Tlaxcala-Puebla s/n, Colonia Xicohténcatl, Apdo. Postal 262, Tlaxcala, Tlaxcala 90070, México, e-mail: [email protected] Abstract: Animal-pollinated angiosperm plants that respond positively to nectar removal by replenishment invest energy that can entail a reproductive cost. Here we use nectar removal manipulation to investigate whether nectar removal increases total nectar production in Moussonia deppeana (Gesneriaceae) and to see if this leads to lower seed production. We found that flowers strongly respond to increased nectar removal by producing 2–4 times as much additional nectar. Other nectar removal treatments had little effect on nectar production and rule out alternative explanations at the flower level. Compared with open-pollinated flowers, hand cross-pollination yielded similar seed production in flowers with experimentally increased nectar removal. Although flower-level effects of nectar replenishment on seed production were not detected in M. deppeana, costs of nectar replenishment need further study as tradeoffs between nectar production and seed production could be expressed at the plant level and/or as long-term effects. Keywords: Gesneriaceae, nectar production, nectar removal, nectar replenishment, protandry. Résumé : Les plantes angiospermes à pollinisation par les animaux qui répondent positivement au retrait de nectar par le réapprovisionnement investissent de l’énergie ce qui peut entraîner un coût reproductif. Dans une expérience de manipulation, nous avons utilisé le retrait de nectar afin d’étudier si le retrait cause une augmentation de la production total de nectar chez Moussonia deppeana (Gesneriaceae) et pour vérifier si cela conduit à une diminution de la production de graines. Nous avons observé que les fleurs répondent fortement à l’augmentation du retrait de nectar en produisant de 2 à 4 fois plus de nectar. Les autres traitements de retrait de nectar avaient peu d’effets sur la production de nectar ce qui exclut les explications alternatives au niveau de la fleur. Pour les fleurs ayant subit une augmentation expérimentale du retrait de nectar, la pollinisation croisée manuelle résultait en une production de graines similaire à celle des fleurs à pollinisation libre. Même si aucun effet du réapprovisionnement en nectar sur la production de graines n’a été détecté au niveau de la fleur chez M. deppeana, il est nécessaire de poursuivre l’étude des coûts du réapprovisionnement en nectar puisque des compromis entre la production de nectar et de graines peuvent exister au niveau de la plante ou à plus long terme. Mots-clés : Gesneriaceae, production de nectar, protandrie, réapprovisionnement en nectar, retrait de nectar. Nomenclature: Wiehler, 1975; 1982. Introduction Documentation of the effects of nectar removal on sub- where nectar tends to evaporate (Castellanos, Wilson & sequent nectar production is interesting from a plant–pol- Thomson, 2002). Replenishment of sugar and water may be linator interaction perspective. Flowers of several plant favoured if male or female reproductive success increases species replenish both volume and sugar after repeated with an increased number of pollinator visits or number removal. Previous studies have shown that experimental of probes by the pollinator (Mitchell, 1993). Under those nectar removal typically increases total nectar produc- circumstances, high replenishment rates would be poten- tion (reviewed in Castellanos, Wilson & Thomson, 2002; tially advantageous, maximizing pollen movement and Ordano & Ornelas, 2004), but the adaptive function, if consequently male and female reproductive success (see any, needs further research. Flowers pollinated over a long also Ordano & Ornelas, 2005). Lastly, low replenishment period of time would benefit by replenishing removed rates may encourage pollinators to revisit plants while keep- nectar (at least water in nectar) when plants are subject to ing the rate of geitonogamy low (Harder & Barrett, 1996). low pollinator visitation rates, particularly in environments Animal-pollinated angiosperm plants that respond positively to nectar removal by replenishment invest energy that can entail a reproductive cost (reviewed in Castellanos, Wilson 1Rec. 2006-02-20; acc. 2006-09-19. & Thomson, 2002; Ordano & Ornelas, 2004). There are Associate Editor: Johan Ehrlén. few studies investigating nectar production costs. Previous 2Author for correspondence. studies have shown that the expenses of nectar produc- ORNELAS, ORDANO & LARA: NECTAR REMOVAL EFFECTS IN MOUSSONIA DEPPEANA tion are negligible in terms of investment in floral tissue or visitation (Alexander, 1990; Jennersten & Kwak, 1991; vegetative growth (Harder & Barrett, 1992; Golubov et al., Shykoff & Bucheli, 1995). (5) Responses to nectar removal 2004; Leiss, Vrieling & Klinkhamer, 2004), but reasonably manipulation seem to be stronger for species pollinated by high in terms of energy investment, photosynthate assimila- hummingbirds inhabiting wet tropical habitats (Ordano & tion (Pleasants & Chaplin, 1983; Southwick, 1984), or seed Ornelas, 2004). Thus, this hummingbird-pollinated species production (Pyke, 1991; Ordano & Ornelas, 2005). Yet we is a good model for examining reproductive costs and rela- know little about the reproductive costs of nectar replen- tionships among energy allocation to nectar reproduction ishment. Ordano and Ornelas (2005) investigated whether that might contribute to a broader understanding of how or not seed production was affected by replenishing nectar fungi exploit pollination systems. in two bromeliad hummingbird-pollinated Tillandsia spe- To determine the effects of repeated removal on total cies that respond strongly and positively to repeated nectar nectar production and the effects of replenishing removed removal (Ordano & Ornelas, 2004). Tillandsia deppeana nectar on seed production in Moussonia deppeana, we set the same number of seeds of the same size regardless of addressed the following questions: (1) Do flowers respond whether or not it had to replenish nectar. In contrast, T. mul- positively to repeated nectar removal by increasing total ticaulis set about half as many seeds when it had to replen- nectar production? And (2) does experimentally increased ish as when it did not. These contrasting results suggest that nectar replenishment affect seed production? the female reproductive costs of nectar replenishment can range from costly to beneficial depending on the identity of Methods the pollinators and changes in their abundance, the habitat and breeding system of the plant, and the level at which STUDY AREA AND SPECIES reproduction is analyzed (McDade & Weeks, 2004; Ordano The study area was the fragmented landscape of tropi- & Ornelas, 2004; 2005). Consequently, there is conflicting cal montane cloud forests near Xalapa City, Veracruz, evidence in terms of reproductive fitness for the broadly Mexico (19° 30' N, 96° 57' W). We worked with a small assumed expenses in nectar production. Moussonia population (∼ 300 plants) growing in shaded Here, we used the same approach to increase nectar areas of a remnant of cloud forest (29 ha) in the Parque production in Moussonia deppeana (Schlecht. & Cham.) Ecológico Francisco Xavier Clavijero (at 1 225 m asl). Hanst. (Gesneriaceae), a hummingbird-pollinated perennial Mean annual precipitation is 1 500 mm, and mean shrub (Lara & Ornelas, 2003). This system is particularly annual temperature is 18 °C. The climate is mild and well suited for an investigation of the effects of replenish- humid throughout the year, with a dry, cold season from ing removed nectar on seed production for several reasons. November to March. A full description of the area is given (1) This gesneriad is protandrous and produces many seeds by Castillo-Campos (1991). Fieldwork was conducted per fruit (Lara & Ornelas, 2003), so effective transfer of from January to April in 2002 and 2003. pollen is important for its reproductive success. If plant Moussonia deppeana (Gesneriaceae) (hereaf- reproductive success increases with increasing pollen depo- ter Moussonia) is an abundant, 1- to 3-m-tall perennial sition, plants would be selected to replenish nectar after its subshrub distributed in forests from southern Mexico to removal by pollinators. (2) The plants are non-autogamous Honduras (Wiehler, 1982). Plants grow solitarily and flower and self-compatible but benefit from producing few flow- from November to April. The axillary inflorescences have ers at day and thus reducing chances for geitonogamous pronounced peduncles with compound cymes of 4 flow- crosses. (3) Flowers produce copious amounts of nectar ers each (Wiehler, 1975). On average, plants open 8 flow- compared to bee-pollinated gesneriads (Stiles & Freeman, ers daily at mid-flowering season (mean ± SD, 8.01 ± 3.5, 1993; Buzato, Sazima & Sazima, 2000). (4) An anther n = 20; Lara & Ornelas, 2001). The orange-red, tubular smut fungus infects Moussonia plants, modifying floral and flowers (∼ 32 mm) are pollinated by the amethyst-throated reproductive characteristics of
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