Nectar Oasis Produced by Agave Marmorata Roezl. (Agavaceae) Lead to Spatial and Temporal Segregation Among Nectarivores in the Tehuaca´N Valley, Me´Xico
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Journal of Arid Environments (2002) 52: 37–51 doi:10.1006/jare.2002.0971, available online at http://www.idealibrary.com on Nectar oasis produced by Agave marmorata Roezl. (Agavaceae) lead to spatial and temporal segregation among nectarivores in the Tehuaca´n Valley, Me´xico Juan Francisco Ornelas*, Mariano Ordano, Ange´lica Herna´ndez, Juan Carlos Lo´pez, Luis Mendoza & Yareni Perroni Departamento de Ecologı´a y Comportamiento Animal, Instituto de Ecologı´a, A.C., Apartado Postal 63, Xalapa, Veracruz 91070, Me´xico (Received 10 August 2001, accepted 2 January 2002) We investigated temporal and spatial segregation of nectarivores at Agave marmorata inflorescences in Tehuaca´n, Me´xico. Using survival analysis, a technique in which data are treated as censored, we found temporal segregation among insects, hummingbirds, and perching birds during the most nectar-limited time. Survivorship curves of hummingbirds and orioles were not significantly different from each other, however, temporal segregation was observed within hummingbirds according to body size and territorial behavior. Temporal segregation among hummingbirds is inter- preted as a way to reduce risk of injury. This way hummingbirds meet their short-term energy demands and co-existence may be facilitated in a nectar oasis. In contrast, survivorship curves of oriole species were not statistically different with each other, but spatial segregation is suspected; Scott’s Orioles segregate by visiting agaves with taller inflorescences sooner than visiting those with shorter inflorescences. These results along with those of foraging behavior and floral shifts suggest that orioles are the legitimate pollinators of this century plant. # 2002 Elsevier Science Ltd. Keywords: Agavaceae; diurnal pollinators; hummingbirds; Me´xico; orioles; nectarivores; survival analysis; Tehuaca´n Valley Introduction Nectarivorous assemblages typically composed by either bees, hawkmoths, humming- birds, passerine birds, and/or bats sharing resources over time, have been widely documented in the literature (Alcorn et al., 1961; Lyon & Chadek, 1971; Borrero, 1972; Primack & Howe, 1975; Cruden & Toledo, 1977; Toledo, 1977; Boyden, 1978; Des Granges, 1978; Carpenter, 1979; Feinsinger et al., 1979; Herna´ndez & Toledo, 1979, 1982; Morton, 1979; Schaffer et al., 1979; Steiner, 1979; Kodric-Brown & Brown 1979; Toledo & Herna´ndez, 1979; Gill et al., 1982; Kuban et al., 1983; *Corresponding author. Fax: (52) (228) 818-7809. E-mail: [email protected] 0140-1963/02/010037 + 15 $35.00/0 # 2002 Elsevier Science Ltd. 38 J.F. ORNELAS ET AL. Schluter, 1986; Eguiarte & Bu´rquez, 1987; Eguiarte et al., 1987; Martı´nez del Rio & Eguiarte, 1987; Gryj et al., 1990; Westerkamp, 1990; Sazima et al., 1993; Sazima & Buzato, 1994; Buzato et al., 1994; Fleming et al., 1996). Researchers have concentrated most of their attention on describing how distantly related taxa partition nectar resources and describing their role as pollinators. In this paper, we present data from a diverse and distantly related assemblages of nectarivores feeding from century plants, but focused on the relative importance of temporal segregation during the most nectar-limited time in the semi-arid Tehuaca´n Valley. This study is a starting point to generate hypotheses about the processes affecting the structure of this community of nectarivores. Methods Study site The study was carried out in the Tehuaca´n Valley (181200N, 971280W; at 1700 m a.s.l.), Puebla, Me´xico. Data were collected in May of 2000 near the city of Tehuaca´n (km 48 Puebla-Oaxaca 135 road), in a flat, rocky area dominated by Yucca periculosa, Agave marmorata, Euphorbia antisiphyllitica, Opuntia pilifera, Pachycereus hollianus, Myrtillocactus geometrizans, Acacia constricta, Mimosa luisana,andProsopis laevigata (Da´vila et al., 1995). The region owes its aridity to the rain shadow produced by the Eastern Sierra Madre (Smith, 1965). Most rain occurs during summer time (Da´vila et al., 1995). It has an average rainfall of 400 mm, an annual mean temperature of 211C, and rarely freezes (Garcı´a, 1973). The main vegetation type is an arid tropical scrub (‘matorral xero´filo’; Rzedowski, 1978) in which succulent forests of columnar cacti with densities of up to 1200 individuals haÀ1 constitute dominant elements in some areas of the valley (Valiente-Banuet & Ezcurra, 1991). Avifauna is composed by a mix of species typically distributed along the Chihuahuan and Sonoran Deserts that have their southernmost distribution in the Tehuaca´n Valley, endemics to the Balsas drainage and the Tehuaca´n–Cuicatla´n Valley, and local migrants from adjacent tropical deciduous forests and pine–oak woodlands to the Tehuaca´n Valley (Arizmendi & Espinosa de los Monteros, 1996). Most columnar cacti provide birds and bats with nectar in the spring (more than 50% of potential reproductive individuals are flowering by April; Valiente-Banuet et al., 1997; J. Garcı´a, pers. comm.), and depend on them for pollination and seed dispersal ( Valiente-Banuet et al., 1996, 1997). Later in the year, when nectar resources from columnar cacti run out, agaves may help to maintain the resident bat population (85% of 19 agave species flower between June and November; Da´vila et al., 1995; S. Arizaga, unpublished data). Flowering of A. macroacantha spans from June to July (Arizaga, 2000) and in some areas coexist with A. marmorata (S. Arizaga, pers. comm.). During our study (May), the only major species that flowered was Agave marmorata (Agavaceae). Alternate resources during this time of year include bee-pollinated Opuntia pilifera (Cactaceae) and hummingbird-pollinated Pedilanthus cymbiferus (Euphorbiaceae), but the amount of nectar offered is minimal ( J. F. Ornelas, pers. obs.). Therefore, the nectar that is offered by agaves between late April and early June ( J. Garcı´a, pers. comm.) represents a nectar oasis to nectar-feeding animals. Study species Agave marmorata Roezl. is a frost-sensitive, obligately outcrossed, semelparous, large agave belonging to the subgenus Agave, group Marmoratae (Gentry, 1982). Commonly found in semi-arid areas in Central Me´xico (Puebla and Oaxaca), NECTAR OASIS AND TEMPORAL SEGREGATION AMONG NECTARIVORES 39 A. marmorata is characterized by a grayish marble-like hue and scabrous leaves (100– 135 cm) with crenate margins and small terminal spines (Gentry, 1982). At the end of its life cycle, each rosette produces a E6-m paniculate inflorescence. The inflorescence has a central stalk branching with 20–25 large diffuse decompound umbels in upper half of the shaft (Gentry, 1982). The bright yellow flowers with small tubes (14–16 mm; M. Ordano, unpublished data) are protandrous and flower characteristics suggest bat pollination (Faegri & Van der Pijl, 1971; Gentry, 1982). Flowers (tubes 5–6 mm deep and 12 mm wide; Gentry, 1982) are open four days and, if not pollinated absise by the sixth day. On the first day, the style is very short (mean 7 S.E. = 45?33 7 1Á03 mm, n = 61 flowers), and the stigmatic lobes are closed. By late afternoon, stamens are fully extended (mean 7 S.E. = 69Á63 7 0Á54 mm, n = 61) and anthers open offering large amounts of yellow pollen until the end of the next day. By the end of the second day, the style grows beyond the stamens (mean 7 S.E. = 85Á33 7 1Á43 mm, n = 61) and the stigmatic surface begins to open. Anther dehiscence occurs E 24 h prior to stigma receptivity (M. Ordano, pers. obs.). Stigmas are receptive during day hours of the second day and the receptivity increases over the day. The proportion of receptive stigmas range from 17 to 20 early in the day (0700– 1000) and from 50 to 80 in the afternoon (1300–1600); most stigmas become receptive by 2300 (M. Ordano, unpublished data). Standing pollen crops were higher in morning hours (31% of stamens sheding pollen), decreased by midday (10%), then increased at night (58%). More pollen is available at night and the decrease by mid- afternoon matches the increase in stigma receptivity (50% of receptive stigmas) (M. Ordano, unpublished data). Although nectar production is higher at night (576Á61 ml flowerÀ112 hÀ1; Benı´tez et al., 1998), flowers produce considerable amounts of nectar over the day. During day hours, standing nectar crops range from 0?2to1?14 ml flowerÀ1 and sugar concentration from 9% to 37% (BRIX) (M. Ordano, unpublished data). Staminate flowers produce more nectar and more concentrated than pistillate flowers (Benı´tez et al. 1998; M. Ordano, unpublished data). Pollen and nectar-feeding bats and sphingid moths have been observed using flowers of A. marmorata (Rojas-Martı´nez & Valiente-Banuet, 1996; A. Rojas- Martı´nez, pers. comm.). Diurnal floral visitors presumably use the remnant nectar that is not consumed by nocturnal visitors (Slauson, 2000). Legitimate pollinators are unknown. The flowering period of A. marmorata spans from end of the dry season (May) to the beginning of the rainy season ( June). In 2001, individuals of A. marmorata flowered earlier in the year (March–May) ( J. F. Ornelas, pers. obs.). Temporal patterns of visitation We haphazardously selected 10 out of the only 35 flowering agaves available in the study area (E100 ha) to observe floral visitors over the course of a day (May 1, 2000). For each plant, we recorded every single foraging event throughout the observation period (0930–1630; 70 h of sampling effort), and noted the species, time of day, foraging behavior, and aggressive interactions. Data were also collected on animals to determine their role as pollinators; the most likely to transfer pollen from one flower to the receptive stigma of another. Observations were performed E10 m away from the focal inflorescence. Approach and avoidance behavior by birds was not detected during observations. Visits by nectar feeding bats and sphingid moths were brief but we were able to determine by visual observation (or binoculars) whether stigma contact was made. Nocturnal observations were made very close to the plants and directing a light source to the umbels. We used Survival Analysis (also known as ‘failure time analysis’) to explore temporal segregation among nectarivores (Abacus Concepts, Inc., 1996).